effects of a secure attachment relationship …allanschore.com/pdf/schoreimhjattachment.pdf · ·...

IMHJ (Wiley) RIGHT INTERACTIVE

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INFANT MENTAL HEALTH JOURNAL, Vol. 22(1–2), 7–66 (2001)� 2001 Michigan Association for Infant Mental Health

A R T I C L E

EFFECTS OF A SECURE ATTACHMENT

RELATIONSHIP ON RIGHT BRAIN DEVELOPMENT,

AFFECT REGULATION, AND

INFANT MENTAL HEALTH

ALLAN N. SCHOREDepartment of Psychiatry and Biobehavioral Sciences

University of California at Los Angeles School of Medicine

ABSTRACT: Over the last ten years the basic knowledge of brain structure and function has vastly ex-panded, and its incorporation into the developmental sciences is now allowing for more complex andheuristic models of human infancy. In a continuation of this effort, in this two-part work I integratecurrent interdisciplinary data from attachment studies on dyadic affective communications, neuroscienceon the early developing right brain, psychophysiology on stress systems, and psychiatry on psychopath-ogenesis to provide a deeper understanding of the psychoneurobiological mechanisms that underlie infantmental health. In this article I detail the neurobiology of a secure attachment, an exemplar of adaptiveinfant mental health, and focus upon the primary caregiver’s psychobiological regulation of the infant’smaturing limbic system, the brain areas specialized for adapting to a rapidly changing environment. Theinfant’s early developing right hemisphere has deep connections into the limbic and autonomic nervoussystems and is dominant for the human stress response, and in this manner the attachment relationshipfacilitates the expansion of the child’s coping capcities. This model suggests that adaptive infant mentalhealth can be fundamentally defined as the earliest expression of flexible strategies for coping with thenovelty and stress that is inherent in human interactions. This efficient right brain function is a resiliencefactor for optimal development over the later stages of the life cycle.

RESUMEN: En los ultimos diez anõs el conocimiento ba´sico de la estructura y funcioń del cerebro se haexpandido considerablemente, y su incorporacioń como parte de las ciencias del desarrollo permite ahoratener modelos de infancia humana ma´s complejos y heurı´sticos. Como una continuacioń a este esfuerzo,en este ensayo que contiene dos partes, se integra la actual informacioń interdisciplinaria que provienede los estudios de la unioń afectiva en relacioń con comunicaciones afectivas en forma de dıádas, laneurociencia en el desarrollo inicial del lado derecho del cerebro, la sicofisiologıá de los sistemas detension emocional, ası´ como la siquiatrıá en cuanto a la sicopatogeńesis, con el fin de presentar unconocimiento ma´s profundo de los mecanismos siconeurobiolo´gicos que sirven de base para la saludmental infantil. En este ensayo se explica con detalle la neurobiologıá de una relacioń afectiva segura,un modelo de salud mental infantil que se puede adaptar, y el enfoque del mismo se centra en la regla-mentacioń sicobiologica que quien primariamente cuida del ninõ tiene del maduramiento del sistemalımbico del infante, o sea, las a´reas del cerebro especialmente dedicadas a la adaptacioń a un medio

Direct correspondence to: Allan N. Schore, Department of Psychiatry and Biobehavioral Sciences, UCLA School ofMedicine, 9817 Sylvia Avenue, Northridge, CA 91324; fax: (818) 349-4404; e-mail: [email protected].

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IMHJ (Wiley) LEFT INTERACTIVE

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cap heightbase of textambiente que cambia ra´pidamente. El temprano desarrollo del hemisferio cerebral derecho del infante

presenta profundas conexiones en cuanto a los sistemas nerviosos lı´mbico y autonomo, y es responsablepor la respuesta humana a la tensioń. De esta manera la relacioń afectiva facilita la expansioń de lashabilidades del ninõ de enfrentar diferentes situaciones. Este modelo sugiere que la salud mental infantilcapaz de ser adaptada puede ser fundamentalmente definida como la expresioń mas temprana de estra-tegias flexibles para enfrentarse con lo novedoso y con la tensioń inherente en las interacciones humanas.Esta efectiva funcioń del lado derecho del cerebro es un factor de resistencia para el desarrollo o´ptimoen los niveles posteriores del ciclo vital.

RESUME: Pendant ces dix dernie`res anneés la connaissance de base de la structure et de la fonction ducerveau s’est conside´rablement accrue, et son incorporation dans les sciences du de´veloppement autorisemaintenant des mode`les plus complexes et heuristiques de la petite enfance humaine. Dans un effort depoursuite de cet effort, j’inte`gre dans ce travail divise´ en deux parties des donneés interdisciplinairesactuelles issues d’e´tudes sur l’attachement des communications affectives dyadiques, la neuroscience surle developpement prećoce de l’he´misphere droit du cerveau, la psychophysiologie sur les syste`mes destress, et la psychiatrie sur la psychopathogeńese de façon aoffrir une compre´hension plus approfondiedes mećanismes psychoneurobiologiques qui sous-tendent la sante´ mentale infantile. Dans cet article jedetaille la neurobiologie d’un attachement solide, un mode`le de sante´ mentale adaptative, et je metsl’accent sur la re´gulation psychobiologique que fait le mode de soin principal du syste`me limbique arrivanta maturitedu petit enfant, les re´gions du cerveau spećialisees dans l’adaptation a` un milieu changeantrapidement. Le de´veloppement prećoce de l’he´misphere droit du petit enfant a de profondes connexionsdans les syste`mes nerveux limbiques et autonomiques et l’emporte pour la re´ponse humaine au stress, etde cette manie`re la relation d’attachement facilite l’expansion des capacite´s afaire face de l’enfant. Cemodele sugge`re que la sante´ mentale adaptive infantile peut eˆtre fondamentalement de´finie commel’expression la plus prećoce de strate´gies flexibles pour faire face a` la nouveaute´ et au stress qui sontinherents aux interactions humaines. Cette fonction efficace de l’he´misphere droit du cerveau est unfacteur de ressort pour le de´veloppement optimal lors des stades ulte´rieurs du cycle de vie.

ZUSAMMENFASUNG: In den letzten zehn Jahren hat sich die grundlegende Kenntnis der Gehirnstrukturund—funktion eindrucksvoll erweitert. Ihre Einbindung in die Entwicklungswissenschaften erlaubt esnun komplexere und erprobbare Modelle der menschlichen Kleinkindzeit zu entwickeln. In Fortsetzungdieser Anstrengungen integriere ich—in dieser zweiteiligen Arbeit—gegenwa¨rtige interdisziplina¨re Er-gebnisse aus Bindungsstudien u¨ber dyadische, gefu¨hlsgesteuerte Kommunikation, aus der Neurologieuber die sich fru¨h entwickelnde rechte Gehirnha¨lfte, aus der Psychophysiologie u¨ber Stresssysteme undaus der Psychiatrie zur Psychopathogenese, um ein tieferes Versta¨ndnis der psychoneurobiologischenMechanismen, die der seelischen Gesundheit des Kleinkinds zugrunde liegen, zu ermo¨glichen.

In dieser Arbeit zeige ich die Neurobiologie der sicheren Bindung auf, ein Beispiel der Anpassungin der seelischen Gesundheit des Kleinkinds und ich beziehe mich auf die psychobiologische Regulationdes kindlichen limbischen Systems durch die prima¨re Bezugsperson. Das limbische System ist jeneGehirnregion, die speziell fu¨r die Anpassung an eine sich schnell a¨ndernde Umgebung zusta¨ndig ist. Diesich schnell entwickelnde rechte Hirnha¨lfte des Kleinkinds hat bedeutende Verbindungen zu dem lim-bischen und dem autonomen Nervensystem und ist bestimmend fu¨r die menschliche Stressreaktion, wo-durch die Bindung die kindlichen Anpassungsleistungen erleichtert. Dieses Modell unterstell, dass dieangepasste seelische Gesundheit des Kleinkinds im Grunde so definiert werden kann: Es ist das ersteAuftauchen der flexiblen Strategien, um mit Neuem auszukommen und zeigt, dass Stress zur men-schlichen Interaktion dazugeho¨rt. Diese effiziente Funktion der rechten Gehirnha¨lfte ist eine Bedingungfur die optimale Entwicklung im weiteren Leben.

Attachment Relationship on Right Brain Development ● 9


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The fundamental importance of the psychological as well as the biological health of theinfant has long been held as a cardinal principle by every clinical discipline that deals withyoung children—infant psychiatry, behavioral pediatrics, child psychology, developmentalpsychoanalysis, and more recently, the emerging fields of developmental psychopathology andinfant mental health. And yet a more precise characterization of the concept of infant mentalhealth, like the definition of “mental health” itself, has been elusive. Theoretically, it is clearthat there must be links between infant and adult mental health, yet these too have been ill-defined. Although there is a large body of clinical knowledge in psychiatry, abnormal psy-chology, and psychoanalysis affirming the centrality of early relational experiences on enduringadaptive and maladaptive aspects of personality, there has been some question as to the struc-tural mechanisms by which such events positively or negatively influence the process of de-velopment as it continues over the lifespan. In other words, how do the earliest interactionsbetween a maturing biological organism and the social environment influence infant mentalhealth, what are the central functions that define infant mental health, and how does it influencemental health at later stages of development?

The defined mission of theInfant Mental Health Journalis to focus upon infant social-emotional development, caregiver– infant interactions, contextual and cultural influences oninfant and family development, and all conditions that place infants and/or their families at riskfor less than optimal development. In this work I want to suggest that although the uniqueimportance of “optimal development” has long been addressed by the psychological sciences,due to the advances of “the decade of the brain,” developmental neuroscience is now in aposition to offer more detailed and integrated psychoneurobiological models of normal andabnormal development. The incorporation of this information into developmental psychologicalmodels could forge closer links between optimal brain development and adaptive infant mentalhealth, as well as altered brain development and maladaptive mental health.

A theoretical concept that is shared by an array of basic and clinical sciences is the conceptof regulation (Schore, 1994, 1996, 1998d, 1999c, 2000b), and because it integrates both thebiological and psychological realms, it can also be used to further models of normal andabnormal structure– function development, and therefore, adaptive and maladaptive infantmental health. Interdisciplinary research and clinical data are affirming the concept that ininfancy and beyond, the regulation of affect is a central organizing principle of human devel-

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cap heightbase of textopment and motivation. In the neuroscience literature Damasio asserts that emotions are the

highest order direct expression of bioregulation in complex organisms (1998), and that pri-mordial representations of body states are the building blocks and scaffolding of development(1994). Brothers argues that emotion occurs “in the context of evolved systems for the mutualregulation of behavior, often involving bodily changes that act as signals” (1997, p. 123).Emotions and their regulation are thus essential to the adaptive function of the brain, which isdescribed by Damasio:

The overall function of the brain is to be well informed about what goes on in the rest ofthe body, the body proper; about what goes on in itself; and about the environment sur-rounding the organism, so that suitable survivable accommodations can be achieved betweenthe organism and the environment. (1994, p. 90)

In a number of works I have described the earliest ontogeny of these adaptive brain func-tions, and have argued that the essential events that allow for the emergence of the regulatorysystems that control such functions occur during the brain growth spurt (Schore, 1994, 1996,1997b, 1998a, 1998b, 2000b, 2000d). Moreover, I have offered data that suggest that theinceptive stages of development represent a maturational period of specifically the early ma-turing right brain, which dominant in the first three years of human life (Chiron, Nabbout,Lounes, Syrota, & Dulac, 1997; Schore, 1994). The right brain is centrally involved in notonly processing social-emotional information, facilitating attachment functions, and regulatingbodily and affective states (Schore, 1994, 1998a), but also in the control of vital functionssupporting survival and enabling the organism to cope actively and passively with stress (Witt-ling & Schweiger, 1993).

Furthermore, in a series of contributions I have proposed that the maturation of theseadaptive right brain regulatory capacities is experience dependent, and that this experience isembedded in the attachment relationship between the infant and primary caregiver (Schore,1994, 1999b, 2000a, 2000b, in press c). But it is important to point out that this experiencecan either positively or negatively influence the maturation of brain structure, and therefore,the psychological development of the infant. This developmental psychoneurobiologicalmodelclearly suggests direct links between secure attachment, development of efficient right brainregulatory functions, and adaptive infant mental health, as well as between traumatic attach-ment, inefficient right brain regulatory function, and maladaptive infant mental health.

In an attempt to forge these conceptual links more tightly, in this two-part work I willaddress the problem of operationally defining adaptive and maladaptive infant mental healthby integrating very recent data from attachment theory, developmental neuroscience, and de-velopmental psychopathology. The primary goal of this latter field is to characterize the on-tological processes whereby early patterns of individual adaptation evolve into later patternsof adaptation (Cicchetti, 1994), and thereby it investigates the early development of the indi-vidual’s coping systems. In generating models of how early ontogenetic factors predisposehigh-risk individuals to later psychopathologies, this rapidly growing interdisciplinaryapproachis directly inquiring into the mechanisms that account for the continuity between infant mentalhealth and mental health at later points in the lifespan.

An essential principle of the developmental psychopathology perspective is that atypicaldevelopment can only be understood in the context of typical development, and so the focusis on underlying mechanisms common to both. This model suggests that any overarchingconception of early development needs to integrate both the biological and psychologicalrealms, and that it must incorporate models of both adaptive and maladaptive infant mental



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construct—rather, it is more precisely characterized as “psychobiological.”Utilizing such a perspective, in these two articles I will contrast the neurobiology of a

secure attachment, an exemplar of adaptive infant mental, with the neurobiology of an insecuredisorganized/disoriented (“type D”) attachment, the most severe form of attachment pathology.This attachment category is associated with early trauma, and will be presented as a prototypeof maladaptive infant mental health. Throughout, I shall underscore the effects of the care-giver’s stress regulating and dysregulating psychobiological interactions on the infant’s ma-turing coping systems that are organizing in the limbic circuitries of the early developing righthemisphere. An increasing body of evidence indicates that “maternal care during infancy servesto ‘program’ behavioral responses to stress in the offspring” (Caldji, Tannenbaum, Sharma,Francis, Plotsky, & Meaney, 1998, p. 5335).

So in the first of this two-part contribution I will offer an overview of an interdisciplinaryperspective of development, outline connections between attachment theory, stress regulation,and infant mental health, describe the neurobiology of a secure attachment, present models ofright brain, early limbic system, and orbital frontolimbic development, and suggest links be-tween continued orbitofrontal and right brain development and adaptive mental health. In thesecond part of this sequenced work I will offer ideas about how early relational traumaticassaults of the developing attachment system inhibit right brain development, impair affectregulating capacities, and negatively impact infant and adult mental health. These models arepresented for further experimental testing and clinical validation.

OVERVIEW OF AN INTERDISCIPLINARY PERSPECTIVEOF DEVELOPMENT

To date, infant mental health has mostly been described in terms of the presence or absenceof certain psychological functions, but it should be pointed out that these functions are, in turn,the product of biological structural systems that are organizing over the stages of infancy. Suchinternal systems are clearly located in the developing brain, which mediates more complexfunctions, and it is known that the conditions and events occurring in “critical” or “sensitive”early periods of brain development have long-enduring effects. Brazelton and Cramer (1990)note that in critical phases energy is high in the infant and the parent for receptivity to eachother’s cues and for adapting to each other.

From late pregnancy through the second year the brain is in a critical period of acceleratedgrowth, a process that consumes higher amounts of energy than any other stage in the lifespan,and so it requires sufficient amounts of not only nutrients, especially long-chainpolyunsaturatedfatty acids (Dobbing, 1997) but also regulated interpersonal experiences for optimal maturation(Levitsky & Strupp, 1995; Schore, 1994). The critical period concept, now firmly establishedin biology (Katz, 1999), prescribes that “specific critical conditions or stimuli are necessaryfor development and can influence development only during that period” (Erzurumlu &Killackey, 1982, p. 207). But it also suggests that during critical periods brain growth isexquisitely susceptible to adverse environmental factors such as nutritional deficits anddysregulating interpersonal affective experiences, both of which negatively impact infantmental health.

The human brain growth spurt, which is at least 5/6 postnatal, begins in the third trimesterin utero and continues to about 18 to 24 months of age (Dobbing & Sands, 1973). During thisperiod the brain is rapidly generating nucleic acids that program developmental processes at arate that will never again be attained. This massive production of both nuclear and mitochon-drial genetic material in the infant’s brain is directly influenced by events in specifically the

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ment utilize a “transactional model,” which views development and brain organization as “aprocess of transaction between (a) genetically coded programs for the formation of structuresand connections among structures and (b) environmental influence” (Fox, Calkins, & Bell,1994, p. 681). So Sander (2000) formulates a key question for deeper understandings of infantmental health:

To what extent can the genetic potentials of an infant brain be augmented or optimizedthrough the experiences and activities of the infant within its own particular caregivingenvironment? (p. 8)

The interface of nature and nurture occurs in the psychobiological interaction betweenmother and infant, “the first encounter between heredity and the psychological environment”(Lehtonen, 1994, p. 28). According to Cicchetti and Tucker, “Environmental experience is nowrecognized to be critical to the differentiation of brain tissue itself. Nature’s potential can berealized only as it enabled by nurture” (1994, p. 538). The evolution and specification of thispotential is described in the current biological literature:

[O]ne of the most fundamental strategies for biological adaptation in organisms is the abilityof the central nervous system (CNS) to react and modify itself to environmental challenges.There is general agreement that the genetic specification of neuronal structure is not sufficientfor an optimally functional nervous system. Indeed, a large variety of experimental ap-proaches indicate that the environment affects the structure and function of the brain.(Gomez-Pinilla, Choi, & Ryba, 1999, p. 1051)

A large body of evidence supports the principle that cortical and subcortical networks aregenerated by a genetically programmed initial overabundant production of synaptic connec-tions, which is then followed by an environmentally driven process of competitive interactionto select those connections that are most effectively entrained to environmental information.This parcellation, the activity-dependent fine tuning of connections and pruning of surpluscircuitry, is a central mechanism of the self-organization of the developing brain (Chechik,Meilijson, & Ruppin, 1999; Schore, 1994). It is important to emphasize, however, that envi-ronmental experience can either enable or constrain the structure and function of the developingbrain. In other words, early interpersonal events positively or negatively impact the structuralorganization of the brain and its expanding adaptive functional capacities. This clearly implies,in the broadest of terms, a direct relationship between an enabling socioemotional environment,an optimally developing brain, and adaptive infant mental health.

A major conclusion of the last decade of developmental neuroscience research is that thereis now agreement that the infant brain “is designed to be molded by the environment it en-counters” (Thomas et al., 1997, p. 209). The brain is thus considered to be a bioenvironmentalor biosocial organ (Gibson, 1996), and investigators are now exploring the unique domains ofthe “social brain” (Brothers, 1990) and the central role of emotions in social communication(Adolphus, 2000). In applying this principle to social-emotional development, the connectionsbetween the neurobiological concept of “enriched environment” and the psychological conceptof “optimal development” can now be more closely coupled in the psychoneurobiologicalconstruct of a “growth-facilitating” (as opposed to “growth-inhibiting”) interpersonal environ-ment (Greenspan, 1981; Schore, 1994) that positively (or negatively) effects the experience-dependent maturation of the brain.



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that developmental processes can best be understood in terms of a context in which evolvingbiological systems are interacting with the social realm. As Cairns and Stoff describe:

It is necessary to go beyond the conventional notion that biological variables not only influ-ence behavior and environment to themoremodern notion that behavioral and environmentalvariables also impact on biology. Maturation and developmental processes may provide thecommon ground for understanding the process of biological social integration. On the onehand, it is virtually impossible to conceptualize developmental changes without recognitionof the inevitable internal modifications that occur within the organism over time. On theother hand, it is misleading to focus on the individual’s biology in the absence of detailedinformation about the interaction and social circumstances in which the behavior occurs.(1996, p. 349)

This integration of biology and psychology to understand development has a rich traditionin science. InThe Expression of Emotions in Man and Animals, Darwin (1872) established thescientific study of emotions and proposed that movements of expression in the face and bodyserve as the first means of communication between the mother and her infant (Schore, 2000a,2000b, 2000c). And inThe Project for a Scientific Psychology, Freud (1895), in an attempt tolink neurology and psychology, first presented both his models of early development and ideason how early traumatic events could heighten the risk of later forming psychopathology(Schore, 1995, 1997a, 1997c). Although others have followed this line of integrating the bio-logical and psychological realms, perhaps the most important scientist of the late twentiethcentury to apply an interdisciplinary perspective to the understanding of how early develop-mental processes influence later mental health was John Bowlby. Over two decades ago heasserted that attachment theory can frame specific hypotheses that relate early family experi-ences to different forms of psychiatric disorders, including the neurophysiological changes thataccompany these disturbances of mental health. It is thus no coincidence that attachment theory,the dominant theoretical model of development in contemporary psychology, psychoanalysis,and psychiatry, is the most powerful current source of hypotheses about infant mental health.

ATTACHMENT, STRESS REGULATION, AND INFANTMENTAL HEALTH

In his classic work of developmental science Bowlby (1969) called for deeper explorations ofhow an immature organism is critically shaped by its primordial relationship with a matureadult member of its species, that is, more extensive studies of how an attachment bond formsbetween the infant and mother (Schore, 2000a, 2000b). In this conception, developmentalprocesses are the product of the interaction of a unique genetic endowment with a particular“environment of adaptiveness, and especially of his interaction with the principal figure in thatenvironment, namely his mother” (Bowlby, 1969, p. 180). Thus, the infant’s emerging social,psychological, and biological capacities cannot be understood apart from its relationship withthe mother.

More specifically, inAttachment, (1969) Bowlby inquired into the mechanisms by whichthe infant forms a secure attachment bond of emotional communication with the mother, andhow this early socioemotional learning is then internalized in the form of an enduring capacityto regulate and thereby generate and maintain states of emotional security. He observed that

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emotions, happy or the reverse,” (p. 242), that this interaction occurs within a context of “facialexpression, posture, tone of voice, physiological changes, tempo of movement, and incipientaction,” (p. 120), that attachment interactions allow for the emergence of abiological controlsystemthat functions in the organism’s “state of arousal” (pp. 152–157), that the instinctivebehavior that constitutes attachment emerges from the coconstructed environment of evolu-tionary adaptiveness has consequences that are “vital to the survival of the species” (p. 137),and that the infant’s “capacity to cope with stress” is correlated with certain maternal behaviors(p. 344). These last two factors, adaptiveness and coping capacity, are obviously central com-ponents of infant mental health.

In recent writings I have contended that attachment theory is, in essence, a regulatorytheory (Schore, 2000a, 2000b, 2000c). More specifically, in such attachment transactions thesecure mother, at an intuitive, nonconscious level, is continuously regulating the baby’s shiftingarousal levels and therefore emotional states. Emotions are the highest order direct expressionof bioregulation in complex organisms (Damasio, 1998), and attachment can thus be definedas the dyadic regulation of emotion (Sroufe, 1996). As a result of being exposed to the primarycaregiver’s regulatory capacities, the infant’s expanding adaptive ability to evaluate on a mo-ment-to-moment basis stressful changes in the external environment, especially the social en-vironment, allows him or her to begin to form coherent responses to cope with stressors. It isimportant to note that not just painful experiences but novel events are stressors. This meansthat the capacity to orient towards not only the familiar but to approach, tolerate, and incor-porate novelty is fundamental to the expansion of a developing system’s adaptive capacity tolearn new information and, therefore, to move towards more complexity.

Furthermore, because the maturation of the brain systems that mediate this coping capacityoccurs in human infancy, the development of the ability to adaptively copewith stress is directlyand significantly influenced by the infant’s early interaction with the primary caregiver (Schore,1994, 1997b, 2000b). In support of Bowlby’s speculations on the association of attachmentwith coping mechanisms, recent interdisciplinary studies indicate that “even subtle differencesin maternal behavior can affect infant attachment, development, and physical well-being”(Champoux, Byrne, DeLizio, & Suomi, 1992, p. 254), and that “variations in maternal carecan serve as the basis for a nongenomic behavioral transmission of individual differences instress reactivity across generations” (Francis, Diorio, Liu, & Meaney, 1999, p. 1155).

In other words, the same interactive regulatory transactions that cocreate a secure attach-ment bond also influence the development and expansion of the infant’s regulatory systemsinvolved in appraising and coping with stress, and therefore, essential to organismic survival.According to McEwen and Stellar, “A stressful stimulus results in a severe perturbation of anorganism’s physiological systems, and the degree of the perceived or real threat determines themagnitude of the stress response to an internal or extrernal challenge” (1993, p. 2093). Indescribing stress, a concept that lies at the interface of the biological and psychological realms,Weinstock (1997) states:

The survival of living organisms depends upon the maintenance of a harmonious equilibriumor homeostasis in the face of constant challenge by intrinsic or extrinsic forces or stressors.Stress is a term that is widely used to describe both the subjective experience induced by anovel, potentially threatening or distressing situation, and the behavioral or neurochemicalreactions to it. These are designed to promote adaptive response to the physical and psy-chological stimuli and preserve homeostasis. . . . Successful equilibrium is reflected by a



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or gives way to counter-regulatory measures to prevent an excessive reaction. (p. 1)

There is now agreement that the these critical functions are mediated by the sympathetic–adrenomedullary (SAM) axis and the hypothalamo–pituitary–adrenocortical (HPA) axis. Fur-thermore, a growing body of studies indicates that the threshold for stimulation of the SAMaxis is lower than that for stimulation of the HPA axis (Malarkey, Lipkus, & Cacioppo, 1995),and that the neurochemistry of the former is regulated by the major stress hormone, cortico-tropin releasing factor (CRF), that regulates catecholamine release in the sympathetic nervoussystem (Brown, Fisher, Spiess, Rivier, Rivier & Vale, 1982), and of the latter by the gluco-corticoid, cortisol, the major “antistress” hormone (Yehuda, 1999). Yehuda points out that thegreater the severity of the stressor, the higher the levels of these neurochemicals, and also thatthe actions of these two systems are synergistic: “whereas catecholamines facilitate the avail-ability of energy to the body’s vital organs, cortisol’s role in stress is to help contain, or shutdown sympathetic activation” (1999, p. 257).

In other words, the energy-expending sympathetic and energy-conserving parasympatheticcomponents of the autonomic nervous system (ANS) regulate the autonomic, somatic aspectsof not only stress responses but emotional states. This adaptive function is stressed by Porges(1997, p. 65):

Emotion depends on the communication between the autonomic nervous system and thebrain; visceral afferents convey information on physiological state to the brain and are criticalto the sensory or psychological experience of emotion, and cranial nerves and the sympa-thetic nervous system are outputs from the brain that provide somatomotor and visceromotorcontrol of the expression of emotion.

But in addition to the ANS, there is now a growing appreciation of the role of the centralnervous system (CNS) limbic circuits in coping capacities, because this emotion-processingsystem is specialized to appraise social information from facial expressions implicitly, withoutconscious awareness (Critchley et al., 2000a), to represent motivationally salient stimuli toadapt to a rapidly changing environment (Mesulam, 1998), and to alter the activity of brainstem neuromodulatory systems responsible for emotional states and arousal (Tucker, 1992).These subcortically produced neuromodulatory bioamines, especially the catecholamines do-pamine and noradrenaline, regulate brain state (Flicker, McCarley, & Hobson, 1981), energymetabolism (Huang, Peng, Chen, Hajek, Zhao, & Hertz, 1994) and blood flowmicrocirculation(Krimer, Mully, Williams, & Goldman-Rakic, 1998). By activating cAMP-response element-binding protein (CREB; Walton & Dragunow, 2000), they also act as internal clocks to coor-dinate the timing of developmental processes (Lauder & Krebs, 1986) and mediate both trophicgrowth-promoting and stress-related functions (Morris, Seidler, & Slotkin, 1983; O’Dowd,Barrington, Ng, Hertz, & Hertz, 1994; Schore, 1994). The limbic system is involved in stressfunctions (Seyle, 1956), and various components of this system are responsible for appraisingthe salience of a stressor, and then initiating and organizing a psychobiological response.

Current developmental research indicates that individual differences in peripheral and cen-tral autonomic balance emerge in early development, and that these are reflected in the affectiveand cognitive domains (Friedman & Thayer, 1998). The “lower,” subcortical sympathetic andparasympathetic components of the ANS, as well as the “higher” cortical limbic componentsof the CNS, are organizing pre- and postnatally, and their maturation is experience dependent(Schore, 1996, 2000d). In fact it is now thought that

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opment, during which time experience or environmental events might participate in shapingongoing synapse formation. (Rinaman, Levitt, & Card, 2000, p. 2739)

This organization is especially expressed in the early maturing (Chiron et al., 1997) righthemisphere, which, more so than the later developing left, deeply connects into both the limbicsystem (Tucker, 1992) and ANS (Spence, Shapiro, & Zaidel, 1996), and is therefore, dominantfor the human stress response (Wittling, 1997) and organismic survival (Wittling & Schweiger,1993). The environmental events that influence ANS–limbic circuit development are embed-ded in the infant’s ongoing affect regulating attachment transactions. Bowlby suggested thatthe limbic system is intimately tied to attachment, an idea furthered by Anders and Zeanah(1984). But these circuits are emphasized in specifically the right brain, because compared tothe left, “the right limbic system may be better connected with subcortical neurochemicalsystems associated with emotion” (Buck, 1994, p. 272).

It is now accepted that in a growth-facilitating social enviornment the attachment inter-actions the child has with its mediators influences the maturation of connections within herdeveloping limbic system (Schore, 1994), and that cortical paralimbic networks are formedthrough “ontogenetic plasticity, that is, through a natural selection of those connections thatmatch the data in the environment” (Tucker, 1992, p. 109). On the other hand, current devel-opmental neurobiological research reveals that growth-inhibiting, adverse early rearing expe-riences “have longstanding and complex effects on a range of neurochemicals relevant toemotion regulation” (Coplan et al., 1998, p. 473). Severely compromised attachment historiesare thus associated with brain organizations that are inefficient in regulating affective statesand coping with stress (Schore, 1997b), and therefore, engender maladaptive infant mentalhealth. This deficit is expressed in a failure to move away from homeostasis to turn on neu-rochemical stress responses when needed, and/or to turn them off and reestablish homeostasiswhen they are no longer needed.

As Emde (1988) has pointed out, a developmental orientation indictates that maladaptivefunctioning is specifically manifest as a lack of variability when an individual is faced withenvironmental demands that call for alternative choices and strategies for change. In light ofthe principle that the process of reestablishing homeostasis in the face of challenge allows forthe adaptive capacity of “achieving stability through change” (Schulkin, Gold, & McEwen,1998, p. 220), this deficit results in not just an unstable self-system but one with a poor capacityto change, a limited ability to continue to develop at later points in the life cycle. Crittendenand DiLalla describe:

Adaptive development can be considered a product of the interaction of a changing biologicalorganism with its environment such that the organism is effective in using the resources ofits environment to meet its present needs without jeopardizing its future development. Mal-adaptive developmental courses either do not meet the organism’s present needs as well asothers or they reduce the organism’s responsiveness to future change. (1988, p. 585)

This relationship between events in early development and a later capacity for change isdue to the fact that the early social environment directly impacts the experience-dependentmaturation of the limbic system, the brain areas specialized for the organization of new learningand the capacity to adapt to a rapidly changing environment (Mesulam, 1998). Because limbicareas in the cortex and subcortex are in a critical period of growth in the first two years and



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cap heightbase of textthese same neurobiological structures mediate stress-coping capacities for the rest of the the

lifespan, early interpersonal stress-inducing and stress-regulating events have long-enduringeffects.

Indeed, recent developmental psychobiological studies suggest that:

An individual’s response to stressful stimuli may be maladaptive producing physiologicaland behavioral responses that may have detrimental consequences, or may be adaptive,enabling the individual to better cope with stress. Events experienced early in life may beparticularly important in shaping the individual’s pattern of responsiveness in later stages oflife. (Kehoe, Shoemaker, Triano, Hoffman, & Arons, 1996, p. 1435)

This conception suggests direct links between infant and adult mental health.Integrating these conceptualizations, I suggest that adaptive infant mental health can be

fundamentally defined as the earliest expression of efficient and resilient strategies for copingwith novelty and stress, and maladaptive infant mental health as a deficit in these same copingmechanisms. The former is a resilience factor for coping with psychobiological stressors atlater stages of the life cycle, the latter is a risk factor for interruptions of developmental pro-cesses and a vulnerability to the coping deficits that define later-forming psychopathogies. Bothare attachment outcomes, and so this formulation is congruent with Main’s (1996) assertionthat “disorganized” and “organized” forms of insecure attachment are primary risk factors forthe development of mental disorders.

AFFECT SYNCHRONY, RESONANCE, ANDATTACHMENT COMMUNICATIONS

The ontogeny of adaptive infant mental health is positively correlated with the ongoing de-velopment of attachment experiences over the first year. This is due to the fact that the expe-rience-dependent maturation of the baby’s brain allows for the emergence of more complexfunctional capacities for coping with stressors, especially those from the social environment.This developmental advance is an outcome of the cocreation of a secure attachment bond ofemotional communication between infant and mother. It has been said that “learning how tocommunicate represents perhaps the most important developmental process to take place duringinfancy’ (Papousek & Papousek, 1997, p. 42). What do we know about the relationships be-tween the earliest development of socio-emotional communication and the organization ofadaptive brain systems?

From birth onwards, the infant is using its expanding coping capacities to interact withthe social environment. In the earliest proto-attachment experiences, the infant is utilizing itsmaturing motor and developing sensory capacities, especially smell, taste, and touch, to interactwith the social environment. As described by Trevarthen (2000) and confirmed in very recentresearch on rhythmic discriminations in newborns (Ramus, Hauser, Miller, Morris, & Mehler,2000), auditory stimuli are also impacting the infant’s developing sensory systems. But by theend of the second month there is a dramatic progression of its social and emotional capacities.In two functional magnetic resonance imaging (fMRI) studies, Yamada et al. (1997, 2000)demonstrate amilestone for normal development of the infant brain occurs at about eight weeks.At this point a rapid metabolic change occurs in the primary visual cortex of infants. Theseauthors interpret this rise to reflect the onset of a critical period during which synaptic con-nections in the occipital cortex are modified by visual experience.

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cap heightbase of textWith this maturational advance, the visual stimuli emanating from the mother’s emotion-

ally expressive becomes the most potent stimulus in the infant’s social environment, and thechild’s intense interest in her face, especially in her eyes, leads him to track it in space, and toengage in periods of intense mutual gaze. The infant’s gaze, in turn, evokes the mother’s gaze,thereby acting as a potent interpersonal channel for the transmission of “reciprocal mutualinfluences.” In the developmental psychological literature, Fogel and Branco (1997) charac-terize infant emotional metacommunication in parent– infant interaction expressed in nonverbalgaze direction, facial expression, posture, and body movements that are “mutually coordinatedto create emergent social patterns” (p. 68). Writing in the neurobiological literature, Allmanand Brothers assert, “When mutual eye contact is established, both participants know that theloop between them has been closed . . . andthis is the most potent of all social situations”(1994, p. 61).

In very recent basic research on three-month-old infants, Feldman, Greenbaum, and Yir-miya (1999, p. 223) describe:

Face-to-face interactions, emerging at approximately 2 months of age, are highly arousing,affect-laden, short interpersonal events that expose infants to high levels of cognitive andsocial information. To regulate the high positive arousal, mothers and infants . . .synchronize the intensity of their affective behavior within lags of split seconds.

These episodes of “affect synchrony” occur in the first expression of social play, and at thistime they are patterned by an infant-leads-mother-follows sequence. This highly organizeddialogue of visual and auditory signals is transacted within milliseconds, and is composed ofcyclic oscillations between states of attention and inattention in each partner’s play. In thisinteractive matrix both partners match states and then simultaneously adjust their social atten-tion, stimulation, and accelerating arousal to each other’s responses.

Feldman and her colleagues assert,

Synchronicity is defined as a match between mother’s and infant’s activities that promotespositivity and mutuality in play. By synchronizing with the child’s attentive states, mothersstructure playful interactions, regulate infant attention, facilitate the development of verbaldialogue, and promote the infant’s capacity for self-regulation . . . mutual synchrony existswhen both partners simultaneously adjust their attention and stimulation in response to thepartner’s signals. (1996, p. 349)

These are critical events, because they represent a fundamental opportunity to practice theinterpersonal coordination of biological rhythms. According to Lester, Hoffman, and Brazelton“synchrony develops as a consequence of each partner’s learning the rhythmic structure of theother and modifying his or her behavior to fit that structure” (1985, p. 24).

In this process of “contingent responsivity,” not only the tempo of their engagement butalso their disengagement and reengagement is coordinated. The more the psychobiologicallyattuned mother tunes her activity level to the infant during periods of social engagement, themore she allows him to recover quietly in periods of disengagement, and the more she attendsto the child’s reinitiating cues for reengagement, the more synchronized their interaction. Theperiod immediately after a “moment of meeting,” when both partners disengage, provides “openspace,” in which both can be together, yet alone (autoregulating) in the presence of the other(Sander, 1988). The synchronizing caregiver thus facilitates the infant’s information processing



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cap heightbase of textby adjusting the mode, amount, variability, and timing of the onset and offset of stimulation

to the infant’s actual integrative capacities. These mutually attuned synchronized interactionsare fundamental to the healthy affective development of the infant (Penman, Meares, & Mil-grom-Friedman, 1983).

In these exchanges of affect synchrony, as the mother and infant match each other’s tem-poral and affective patterns, each recreates an inner psychophysiological state similar to thepartner’s. Stern (1983b) describes moment-to-moment state sharing, feeling the same as theother, and state complementing, responding in one’s unique way to stimuli coming from theother. In contexts of “mutually attuned selective cueing,” the infant learns to preferentiallysend social cues to which the mother has responded, thereby reflecting “an anticipatory senseof response of the other to the self, concomitant with an accommodation of the self to theother” (Bergman, 1999, p. 96).

In describing the unique nature of an emotionally communicationg mother– infant dyad,a number of prominent theoreticians have been drawn to the concept of resonance. Trevarthendescribes

Corresponding generative parameters in . . . twosubjects enable them to resonate with orreflect on one another as minds in expressive bodies. This action pattern can become “en-trained,” and their experiences can be brought into register and imitated. These are thefeatures that make possible the kind of affectionate empathic communication that occurs,for instance, between young infants and their mothers. (1993, p. 126)

Simliarly, Sander (1991) emphasizes the critical importance of the context of a specificallyfitted interaction between the infant and mother as a resonance between two systems attunedto each other by corresponding properties. Such energy-infused moments allow for a sense ofvitalization, and thereby increased complexity and coherence of organization within the infant.

Furthermore, in the visual and auditory emotional communications embedded within syn-chronized face-to-face transactions, both members of the dyad experience a state transition asthey move together from low arousal to a heightened energetic state of high arousal, a shiftfrom quiet alertness into an intensely positive affective state. In physics, a property of resonanceis sympathetic vibration, which is the tendency of one resonance system to enlarge and augmentthrough matching the resonance frequency pattern of another resonance system. It is wellestablished that energy shifts are the most basic and fundamental features of emotion, that thetransfer of emotional information is intensified in resonant contexts, and that at the momentwhen a system is tuned at the “resonant” frequency it becomes synchronized (Schore, 1997b,2000d, in press a).

Resonances often have chaos associated with them, and thus they are characterized bynonlinear dynamical factors—relatively small input amplitudes engender a response with asurprisingly large output amplitude. This amplification especially occurs when external sensorystimulation frequency coincides with the organism’s own endogenous rhythms. In other words,when a psychobiologically attuned dyad cocreates a resonant context within an attachmenttransaction, the behavioral manifestation of each partner’s internal state is monitored by theother, and this results in the coupling between the output of one partner’s loop and the inputof the other’s to form a larger feedback configuration and an amplification of the positive statein both.

In demonstration of this principle, emotion theorists describe “affect bursts,” nonverbalexpressions of synchronized facial and vocal activity triggered by an external stimulus (Scherer,1994). And infant researchers refer to the delight the infant displays in reaction to the aug-

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cap heightbase of textmenting effects of his mother’s playful, empathically attuned behavior, her mulitmodal sensory

amplification and resonance with the child’s feelings. Stern (1985) describes a particular ma-ternal social behavior that can “blast the infant into the next orbit of positive excitation,” andgenerate “vitality affects.” In these transactions the dyad is cocreating “mutual regulatory sys-tems of arousal” (Stern, 1983a).

In this interactive context, the infant’s attachment motivation synergistically interacts withthe caregiver’s maternal motivation. In current psychobiological models maternal motivationis conceptualized as the outcome of the interaction between external visual and auditory infantstimuli and the central state of maternal arousability (Pryce, 1992). To act as a regulator of theinfant’s arousal, she must be able to regulate her own arousal state. The burgeoning capacityof the infant to experience increasing levels of accelerating, rewarding arousal states is thus atthis stage amplified and externally regulated by the psychobiologically attuned mother, anddepends upon her capacity to engage in an interactive emotion communicating mechanism thatgenerates these in herself and her child.

Reciprocal facial signalling, mutual rhythmic entrainment, and dyadic resonance thus actas a psychobiological context for an open channel of social communication, and this interactivematrix promotes the outward expression of internal affective states in infants. Sander (1997)asserts that the parent expresses a behavior that is particularly fitted to catalyze a shift in theinfant’s state, and Tronick et al. (1998) state that the complexity of the infant’s state is ex-pandable with input from an external source—the caregiver. To enter into this communication,the mother must be psychobiologically attuned not so much to the child’s overt behavior as tothe reflections of the rhythms of his internal state.

Because affect attunements are “spontaneous, nonverbal responses to . . . children’s ex-pressed emotions” (Polan & Hofer, 1999, p. 176), the moment-to-moment expressions of themother’s regulatory functions occur at levels beneath awareness. Even so, the attuned mothercan self-correct by accessing her reflective function whereby she monitors not only her infant’sbut her own internal signals and differentiates her own affective state. As a regulator of theinfant’s arousal levels, she also modulates nonoptimal high levels of stimulation that wouldinduce supraheightened levels of arousal in the infant. Thus, she regulates not just the type butalso the intensity of socioaffective information within the dyad’s communication system.

But the primary caregiver is not always attuned—developmental research shows frequentmoments of misattunement in the dyad, ruptures of the attachment bond. In early developmentan adult provides much of the necessary modulation of infant states, especially after a statedisruption and across a transition between states, and this allows for the development of self-regulation. Again, the key to this is the caregiver’s capacity to monitor and regulate her ownaffect, especially negative affect. The regulation of her own affective state, as well as thechild’s, may be an emotionally demanding task.

In this essential regulatory pattern of “disruption and repair” (Beebe & Lachmann, 1994;Schore, 1994) the “good-enough” caregiver who induces a stress response in her infant througha misattunement, reinvokes in a timely fashion her psychobiologically attuned regulation ofthe infant’s negative affect state that she has triggered. The reattuning, comforting mother andinfant thus dyadically negotiate a stressful state transition of affect, cognition, and behavior.This recovery mechanism underlies the phenomenon of “interactive repair” (Tronick, 1989;Lewis, 2000), in which participation of the caregiver is responsible for the reparation of stressfuldyadic misattunements.

If attachment is interactive synchrony, stress is defined as an asynchrony in an interactionalsequence, but a period of synchrony following this allows for stress recovery (Chapple, 1970).It is now thought that the process of reexperiencing positive affect following negative expe-



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cap heightbase of textriencemay teach a child that negativity can be endured and conquered. Infant resilienceemerges

from an interactive context in which the child and parent transition from positive to negativeand back to positive affect, and resilience in the face of stress is an ultimate indicator ofattachment capacity and therefore adaptive mental health.

These arousal-regulating transactions, which continue throughout the first year, underliethe formation of an attachment bond between the infant and primary caregiver. An essentialattachment function is “to promote the synchrony or regulation of biological and behavioralsystems on an organismic level” (Reite & Capitanio, 1985, p. 235). Indeed, psychobiologicalattunement and the interactive mutual entrainment of physiological rhythms are fundamentalprocesses that mediates attachment bond formation, and attachment can be defined as theregulation of biological synchronicity between organisms (Schore, 2000b; Wang, 1997). Themechanism of attachment dynamics is thus an example of the regulation of rhythm, which isa fundamental organizing principle of all living systems (Iberall & McCulloch, 1969).

To put this another way, the infant’s developing regulatory and control systems createspontaneous physiological rhythms that are manifest in arousal fluctuations, which are in turnexpressed in fluctuating psychobiological affective states, what Stern (1985) calls vitality af-fects. It is now accepted that affects reflect an individual’s internal state and have an hedonic(valenced) dimension and an arousal (intensity) dimension. The crescendos and decrescendosof the infant’s peripheral (ANS) and central (CNS) arousal systems underlie emotions, and sothe mutual entrainment of affective states in attachment transactions can be defined as thedyadic regulation of emotion (Sroufe, 1996). Thus, Damasio (1998) is correct in characterizingemotions as the highest order direct expression of bioregulation in complex organisms, but itshould be emphasized that the efficient bioregulation of internal emotional states can take theform of both interactive regulation and autoregulation.

These data underscore an essential principle overlooked by many emotion theorists—affect regulation is not just the reduction of affective intensity, the dampening of negativeemotion. It also involves an amplification, an intensification of positive emotion, a conditionnecessary for more complex self-organization. Attachment is not just the restablishment ofsecurity after a dysregulating experience and a stressful negative state, it is also the interactiveamplification of positive affects, as in play states. Regulated affective interactions with a fa-miliar, predictable primary caregiver create not only a sense of safety, but also a positivelycharged curiosity that fuels the burgeoning self’s exploration of novel socioemotional andphysical environments (Schore, 1994; Grossman, Grossman, & Zimmerman, 1999). This abilityis a marker of adaptive infant mental health.

ATTACHMENT AND THE INTERACTIVE REGULATIONOF THE RIGHT BRAIN

In a number of contributions I have offered evidence that indicates that the emotional com-munications of evolving attachment transactions directly impact the experience-dependentmat-uration of the infant’s developing brain. Trevarthen (1993) also observes that that the growthof the baby’s brain literally requires brain–brain interaction, and occurs in the context of apositive affective relationship (see Figure 1). But in light of the fact that the early maturingright hemsphere is in a growth spurt in the first year-and-a-half, and that it is dominant for thefirst three (Chiron et al., 1997), I have contended that attachment experiences specificallyimpact the development of the infant’s right brain. Confirming this model, Ryan, Kuhl, andDeci, using EEG and neuroimaging data, now report,

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FIGURE 1.1. Brain–brain interactions during face-to-face communications of proto-conversation, me-diated by eye-to-eye orientations, vocalizations, hand gestures, and movements of the arms and head, allacting in coordination to express interpersonal awareness and emotions. Adapted from Aitken & Trevar-then (1993) and used with permission of Cambridge University Press.

The positive emotional exchange resulting from autonomy-supportive parenting involvesparticipation of right hemispheric cortical and subcortical systems that participate in global,tonic emotional modulation. (1997, p. 719)

In an elegant phrase Trevarthen asserts that “the intrinsic regulators of human brain growthin a child are specifically adapted to be coupled, by emotional communication, to the regulatorsof adult brains” (Trevarthen, 1990, p. 357). But again, I would amend this general statementto suggest that the regulators of both the infant and mother’s brains are located in specificallythe right limbic brain (Schore, 1994). Furthermore, Trevarthen’s description of “emotionalcommunication” as a traffic of visual, prosodic auditory, and gestural signals that induce instantemotional effects is paralleled by Buck’s (1994) characterization of “spontaneous emotionalcommunication”:

Spontaneous communication employs species-specific expressive displays in the sender that,given attention, activate emotional preattunements and are directly perceived by the re-ceiver . . . The“meaning” of the display is known directly by the receiver . . . This spon-taneous emotional communication constitutes aconversation between limbic systems. . . Itis a biologically-based communication system that involves individual organismsdirectlywith one another:the individuals in spontaneous communication constitute literally a bio-logical unit . . . The direct involvement with the other intrinsic to spontaneous commu-nication represents an attachment that may satisfy deeply emotional social motives. (p. 266,my italics)

Buck (1994) emphasizes the importance of the right limbic system, and localizes this biolog-ically based spontaneous emotional communication system to the right hemisphere, in accord


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cap heightbase of textwith other research that indicates a right lateralization of spontaneous gestures (Blonder, Barns,

Bowers, Moore, & Heilman, 1995) and emotional communication (Blonder, Bowers, & Heil-man, 1991).

Recall Winnicott’s (1971) description of the infant’s expression of a “spontaneous ges-ture,” a somato-psychic expression of the burgeoning “true self,” and the attuned mother’s“giving back to the baby the baby’s own self.” Winnicott contends that as a result of itstransactions with the mother, the infant, through identification, internally creates a “subjectiveobject.” Recent research indicates that the right hemisphere is specialized for “the detection ofsubjective objects” (Atchley & Atchley, 1998), and for the processing and regulation of self-related information (Schore, 1994; Ryan et al., 1997; Kennan, Wheeler, Gallup, & Pascual-Leone 2001).

Furthermore, developmental neuroscientists have proposed that engrams related to emo-tional voices are more strongly imprinted into the early maturing, more active right hemisphere(Carmon & Nachson, 1973), and that particular areas of the right hemisphere are timed to bein a plastic and receptive state at the very time when polysensory information that emanatesfrom faces is being attended to most intensely by the infant (Deruelle & de Schonen, 1998; deSchonen, Deruelle, Mancini, & Pascalis, 1993). These latter authors report that right hemisphereactivation in face processing shows a significant structural advance at two to three months, inline with the previously cited work of Yamada et al. (1997, 2000) and Feldman et al. (1999).With ongoing episodes of affective synchrony, attachment functions mature later in the firstyear, and it has been suggested that “there is earlier maturation of right hemisphere inhibitionover subcortically mediated emotional expressions in infancy, once cortical influences overthis behavior come into play” (Best & Queen 1989, p. 273).

An accumulating body of evidence indicates that the infant’s right hemisphere is involvedin attachment and the mother’s right hemisphere in comforting functions (Henry, 1993; Horton,1995; Schore, 1994, 1998a, 1998b, 1999d, Shapiro, Jamner, & Spence, 1997; Siegel, 1999,Wang, 1997). Attachment represents the regulation of biological synchronicity between orga-nisms, and imprinting, the learning process that mediates attachment, is defined as synchronybetween sequential infant–maternal stimuli and behavior (Petrovich & Gewirtz, 1985). Duringthe sequential signalling of play epsiodes mother and infant show sympathetic cardiac accel-eration and then parasympathetic deceleration in response to the smile of the other (Donovan,Leavitt, & Balling, 1978). Imprinting is thus not a unidirectional learning process by whichattachment experiences are passively absorbed into an empty template. Rather, it is an activedyadic process that occurs between two brains that are cogenerating synchronized emotionalcommunications with each other.

I suggest that when two right brain systems are mutually entrained in affective synchronythey create a context of resonance, which is now thought to play a fundamental role in brainorganization, CNS regulatory processes, and the organization of connectivity properties thatare tuned by function (Salansky, Fedotchev, & Bondar, 1998). Earlier I described how in face-to-face contexts resonant amplification occurs when the frequency patterns of the mother’sexogenous sensory stimulation coincides with the infant’s own endogenous organismicrhythms. Trevarthen (1993) points out that the resonance of the dyad ultimately permits theintercoordination of positive affective brain states.

In current neuroscience, resonance refers to the ability of neurons to respond selectivelyto inputs at preferred frequencies, and “amplified resonance” or “amplifying currents” serve asa substrate for coordinating (synchronizing) patterns of network (circuit) activity. Basic re-search establishes that different behavioral and perceptual states are associated with differentbrain rhythms, that a resonant system evolves continuously into a spontaneously oscillatory systemas the amplifying conductance is increased, and that amplified resonance can “tune networks tooperate in frequency ranges of special biological meaning” (Hutcheon & Yarom, 2000, p. 220).


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cap heightbase of textThese general principles apply to face-to-face transactions, where patterns of information

emanating from the caregiver’s face, especially of low visual and auditory frequencies, arespecifically processed by the infant’s right hemisphere (Ornstein, 1997). The ventral stream(Ungerleider & Haxby, 1994) of this hemisphere is specialized to analyze low frequencies ofvisual perception that convey the general outlines of faces and low frequencies of auditorytones that express the emotional intonation of language, prime examples of biologically mean-ingful information. Fernald (1992) describes human maternal vocalizations to infants as “bio-logically relevant signals.” Furthermore, these dyadically synchronized affectively chargedtransactions elicit high levels of metabolic energy for the tuning of right brain cortical–sub-cortical circuits involved in processing socioemotional information (Schore, 1994, 1997b,2000d). An article inSciencesuggests “mothers invest extra energy in their young to promotelarger brains” (Gibbons, 1998, p. 1346).

Lewis (1995) points out that the best example of the flowthrough of energy in a developingsystem is the processing of relevant information in the presence of emotion. Thus, as a resultof synchronized emotional transactions, the organization of the infant’s right brain shows in-creased coherence, as the flow of energy between the hierarchically organized higher rightcortical and lower right subcortical components increase their connectivity, allowing the rightbrain to act as a self-regulating integrated whole, and therefore, capable of increasing com-plexity. This conception is consonant with current models that emphasize that the brain is aself-organizing system (van Pelt, Corner, Uylings, & Lopes da Silva, 1994), and that ageincreases brain complexity (Anokhin, Birnbaumer, Lutzenberger, Nikolaev, & Vogel, 1996).In applying dynamic systems principles to attachment theory, Siegel (1999) proposes a similiarscenario.

The infant’s right brain is tuned to dynamically self-organize upon perceiving certainpatterns of facially expressed exteroceptive information, namely the visual and auditory stimuliemanating from the smiling and laughing joyful face of a loving mother. In face-to-face inter-active affect-amplifying transactions, the relational context triggers facially expressed “affectbursts” in the infant. According to Scherer, these highly emotionally charged events lead to a“strong synchronization of various organismic subsystems, particularly the various expressivechannels, over a very brief period of time” (1994, p. 181).

What psychoneurobiological mechanism could underlie this caregiver-induced organiza-tion of the infant’s brain? In earlier work I have suggested that the appearance of the mother’sface in dyadic play experiences generates high levels of dopaminergic-driven arousal and ela-tion in the infant’s right brain (Schore, 1994). Dopamine neurons in the ventral tegmental areaof the anterior reticular formation are involved in reward and emotionality (Wise & Rompre,1989), and they respond to visual, auditory, and tactile stimuli by switching from “pacemaker-like firing” to “burst firing” (Gonon, 1988; Overton & Clark, 1997) in response to an environ-mental stimulus that is “ethologically salient” (a good definition of sensory stimulation ema-nating from the mother). This pacemaker firing of a subnuclei of arousal-generating ventraltegmental dopamine neurons may represent an important component of the infant’s geneticallyencoded endogenous organismic rhythms.

The bursting of these neurons to salient, arousing environmental stimuli contributes to anorienting response, the setting of a motivational state, and the onset of exploratory behavior(Horvitz, Stewart, & Jacobs, 1997). Furthermore, “electrical coupling among bursting dopa-mine neurons may provide a mechanism for further amplification of the effects of synchro-nously firing dopamine cells on their target areas” (Freeman, Meltzer, & Bunney, 1985, p.1993). Evidence also indicates that the evaluation of an environmental stimulus as affectivelypositive is associated with dopaminergic activation of specifically the right brain (Besson &Louilot, 1995).



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cap heightbase of textAn integration of these data may give us a model of the critical right brain events by which

psychobiologically attuned attachment communications generate amplified resonance that tunesreward circuits to certain forms of human visual and auditory patterns of stimulation. In affec-tively charged face-to-face transactions, the biologically significant information that emanatesfrom the mother’s face is imprinted into the infant’s developing right interior temporal areasthat process familiar faces (Nakamura et al., 2000), and thereby takes on “special biologicalmeaning.” The right hemisphere is also dominant for the perception of “biological motion.”These psychoneurobiological events of mother– infant play sequences drive the “affectivebursts” embedded within moments of affective synchrony, in which positive states of interestand joy are dyadically amplified. Panksepp (1998) contends that “play may have direct trophiceffects on neuronal and synaptic growth in many brain systems” (p. 296), and suggests thatplay serves the adaptive role of organizing affective information in emotional circuits, a func-tion also performed by rapid eye movement (REM) dream sleep. This fits nicely with currentneuroscience conceptions of the important role of REM sleep in brain maturation (Marks,Shaffery, Oksenberg, Speciale, & Roffwarg, 1995) and imaging studies showing a preferentialactivation of limbic regions in REM sleep (Braun et al., 1997; Maquet et al., 1996).

How can we account for the trophic effects of early play episodes? Again, in a previouscontribution (Schore, 1994) I have proposed that in these face-to-face emotional communica-tions, the visual input of the mother’s face is also inducing the production of neuorotrophinsin the infant’s brain, such as brain-derived neurotrophic factor (BDNF). Maternal care has beenshown to increaseN-methyl-D-aspartate (NMDA) receptor levels, resulting in elevated BDNFand synaptogenesis in the infant’s brain (Liu et al., 2000). This trophic factor, which is regulatedby visual input (Gomez-Pinilla et al., 1999), promotes synaptic plasticity during postnatalcritical periods (Huang et al., 1999). BDNF is also a growth-promoting factor formesencephalicdopamine neurons (Hyman et al., 1991), and dopamine, which activates NMDA receptors(Knapp, Schmidt, & Dowling, 1990), is known to perform a growth-promoting role in thepostnatal development of the cortex (Kalsbeek, Buijs, Hoffman, Matthijssen, Pool, & Uylings,1987), especially in corticolimbic areas that send axons down to the dendrites of these dopamineneurons, and thereby come to regulate their activity (Sesack & Pickel, 1992; Schore, 1994).Dopamine acts as a trophic agent via regulation of the developing blood brain barrier (Schore,1994) and microcirculation (Krimer et al., 1998) of developing target areas.

Other psychobiological data may explicate the mechanisms that mediate attachment, theinteractive regulation of biological synchronicity between organisms. Despite the intrinsic dy-adic nature of the attachment concept, hardly any research has concurrently measured motherand infant in the process of interacting with each other. In one of the few studies of this kind,Kalin, Shelton, and Lynn (1995) show that the intimate contact between the mother and herinfant is mutually regulated by the reciprocal activation of their opiate systems—elevatedlevels of beta endorphins increase pleasure in both brains. It is established that opioids enhanceplay behavior (Schore, 1994), and that endorphins increase the firing of mesolimbic dopamineneurons (Yoshida et al., 1993).

Furthering these ideas, the developmental principle of “reciprocal mutual influences” refersto more than mutual behavior changes; indeed, it specifically implies that there are simultaneouschanges within the right brains ofbothmembers of the dyad. In terms of the self-organizationtheory, the mutual entrainment of their right brains during moments of affect synchrony triggersan amplified energy flow that allows for a coherence of organization that sustainsmore complexstates within both the infant’s and the mother’s right brains. In this manner, “the self-organi-zation of the developing brain occurs in the context of a relationship with another self, anotherbrain” (Schore, 1996, p. 60).

Evidence is now appearing that supports the idea that the organization of the mother’s

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cap heightbase of textbrain is also being influenced by these relational transactions. A neurobiological study of early

mammalian mother– infant interactions, published inNature, entitled “Motherhood improveslearning and memory,” reports increased dendritic growth in the mother’s brain (Kinsley et al.,1999). The authors conclude that events in late pregnancy and the early postpartum period

. . . may literally reshape the brain, fashioning amore complex organ that can accommodatean increasingly demanding environment. . . . Toconsider the relationship of a mother car-ing for her young as unidirectional disregards the potentially rich set of sensory cues in theopposite direction that can enrich the mother’s environment. By providing such stimuli,(infants) may ensure both their own and their mother’s development and survival. (p. 137)

Hofer’s (1990) developmental psychobiological work also emphasizes the bidirectionalbrain events of themother– infant interaction. He describes, in detailed fashion, how the infant’simmature and developing internal homeostatic systems are coregulated by the caregiver’smoremature and differentiated nervous system. In this “symbiotic” pleasurable state, the adult’s andinfant’s individual homeostatic systems are linked together in a superordinate organization thatallows for “mutual regulation of vital endocrine, autonomic, and central nervous systems ofboth mother and infant by elements of their interaction with each other” (Hofer, 1990, p. 71).

These matters bear upon the concept of symbiosis, which has had a controversial historyin recent developmental psychoanalytic writings. This debate centers around Mahler, Pine, andBergman’s (1975) reference to a normal symbiotic phase during which the infant “behaves andfunctions as though he and his mother were a single omnipotent system—a dual unity withinone common boundary” (p. 8). Although the symbiotic infant is dimly aware that the motheris the source of his pleasurable experiences, he is in a “state of undifferentiation, a state offusion with the mother, in which the ‘I’ is not differentiated from the ‘not-I’ ” (p. 9).

This latter defintion of symbiosis departs from the classical biological concept, and isunique to psychoanalytic metapsychology. Current evidence may not directly support any in-ferences about the limits of the infant’s awareness, nor about an entire stage that describes theinfant’s behavior only with this characterization. However, moments of face-to-face affectivesynchrony do begin at two to three months, the advent of Mahler’s symbiotic phase, they dogenerate high levels of positive arousal, and such mutually attuned sequences can be portrayedas what Mahler et al. (1975) call instances of “optimal mutual cueing.”

But even more importantly, Hofer’s work as well as recent brain research calls for a returnof the definition of symbiosis to its biological origins. The Oxford dictionary offers the deri-vation from the Greek, “living together,” and defines symbiosis as an interaction between twodissimilar organisms living in close physical association, especiallyone in which each benefitsthe other(my italics). An even more basic definition from biological chemistry suggests that“symbiosis is an association between different organisms that leads to a reciprocal enhancementof their ability to survive” (Lee, Severin, Yokuba Yashi, & Reza Ghadiri, 1997, p. 591). RecallBuck’s (1994) description of an emotionally communicating dyad as “literally a biologicalunit,” a conception that echoes Polan and Hofer’s (1999) description of the dyad as a self-organizing regulatory system composed of mother and infant as a unit. These conceptionssuggest that instances of secure attachment bonding are an example of biological symbiosis.Interestingly, the Oxford dictionary also defines symbiosis as “companion,” which suggeststhat Trevarthen’s concept refers to this same psychobiological phenomenon.

The construct of symbiosis is reflected in the conception of attachment as the interactiveregulation of biological synchronicity between organisms. In discussing the central role offacial signalling in attachment, Cole asserts, “It is through the sharing of facial expressions thatmother and child become as one. It is crucial, in a more Darwinian biological context, for the



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cap heightbase of textinfant to bond her mother to ensure her own survival” (1998, p. 11). Recall Bowlby’s (1969)

assertion that the development of attachment has consequences that are vital to survival andthat the infant’s capacity to cope with stress is correlated with certain maternal behaviors. Theright hemisphere is dominant for both attachment functions and for the control of vital functionssupporting survival and enabling the organism to cope actively and passively with stress. Thesecapacities are surely critical indices of adaptive infant mental health.

ATTACHMENT TRANSACTIONS ANDTHE HIERARCHICAL ORGANIZATION OF

THE LIMBIC SYSTEM

Mary Main concludes that “The formation of an attachment to a specified individual signals aquantitative change in infant behavioral (and no doubt also brain) organization” (1991, p. 214,my italics). As a result of advances in the “decade of the brain” can we now identify whatspecific brain areas mediate this function? In his initial outline of attachment theory, Bowlbyspeculated that a “succession of increasingly sophisticated systems” involving the limbic sys-tem and brain arousal-regulating areas mediate attachment processes (1969, p. 154). It is wellestablished that regions of the brain mature in stages, so the question is, what parts of thepostnatally developing brain are maximally impacted by emotionally charged attachment ex-periences? As previously mentioned, the emotion processing limbic system has been implicatedin attachment functions.

Indeed the first 18 months of human life are critical for the myelination, and therefore, thematuration of particular rapidly developing limbic and cortical association areas and limbicareas of the human cerebral cortex show anatomical maturation at about 15 months. It has longbeen thought that the limbic system is fundamentally associated with emotional functions. Butas I stated previously, recent conceptions emphasize that limbic system function underlies theorganization of new learning and the capacity to adapt to a rapidly changing environment(Mesulam, 1998). This concept relates to Hinde’s assertion that “the development of socialbehavior can be understood only in terms of a continuing dialectic between an active andchanging organism and an active and changing environment” (1990, p. 162).

Within the first year perhaps no organismic system is changing as rapidly as the brain,especially a sequence of ontogenetically appearing limbic circuits. These systems are organizedfrom the simplest to the most complex, and they onset in a fixed progression over the first year,with the later maturing hierarchical cortical structures adaptively regulating the earliermaturingsubcortical systems. This general ontogentic principle is articulated by Werner (1948), whosuggested that “the development of biological forms is expressed in an increasing differentia-tion of parts and an increasing subordination, or hierarchization . . . anordering and groupingof parts in terms of the whole (1948, p. 44). This hierarchical model has been significantlyadvanced in the psychoanalytic literature in the groundbreaking work of Gedo (1999; Gedo &Wilson, 1993).

In the current neuroscience literature Toates describes the importance of hierarchical con-trol systems in development:

Development is associated with gaining autonomy from sensory control and acquisition oftop-down control over behavior that is organized at a lower level. Reflexes can becomeintegrated into cortical control. Such control will be perhaps most usually inhibition, butexcitation might also occur . . . acquisition of higher-level control is not merely a processof more inhibition being exerted since the new forms of reacting to the environment alsoemerge and it is assumed that these are mediated at the higher level. (1998, p. 73)

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FIGURE 2.2. Limbic structures of the right hemisphere, lateral view. Cingulate is labeled limbic cortex(from Trevarthen, Aitken, Papoudi, & Roberts, 1998, and used with permission of Jessica KingsleyPublishers).

In classical ego psychology psychoanalytic writings, Hartmann (1939) proposed that ad-aptation is primarily a reciprocal relationship of the organism and its environment, and thatdevelopment is a differentiation in which primitive regulatory systems are increasingly replacedor supplemented by more effective regulatory systems. The progression and reorganization ofthe infant’s regulatory, control systems is described by Brazelton and Cramer:

The central nervous system, as it develops, drives infants towards mastery of themselvesand their world. As they achieve each level of mastery, they seek a kind of homeostasis,until the nervous system presses them on to their next level. Internal equilibrium is alwaysbeing upset by a new imbalance created as the nervous system matures. Maturation of thenervous system, accompanied by increasing differentiation of skills, drives infants to reor-ganize their control systems (1990, p. 98).

Fischer and Rose (1994) conclude that the development of higher order control systemallows for the emergence of “dynamic skills,” that a developmental stage is a point at whicha new level of control systems emerge, and that emotions fundamentally shape the ways thatcontrol systems develop.

These control systems can now be identified. In current neuroscience, the neuroanatomyof the limbic system is characterized as a hierarchical system of vertically organized circuitswithin the brain (see Figure 2). And so authors are now referring to the “rostral limbic system”



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cap heightbase of texta hierarchical sequence of interconnected limbic areas in orbitofrontal, insular cortex, anterior

cingulate, and amygdala (Devinsky, Morrell, & Vogt, 1995), an “anterior limbic system” com-posed of orbitofrontal cortex, basal forebrain, amygdala, and hypothalamus (Schnider & Ptak,1999), a “paralimbic circuit” containing orbitofrontal, insular, and temporopolar cortices (Me-sulam & Mufson, 1982), an “anterior limbic prefrontal network” interconnecting the orbitaland medial prefrontal cortex with the temporal pole, cingulate, and amygdala (Carmichael &Price, 1995), and a complex circuit of emotion regulation consisting of orbital frontal cortex,anterior cingulate, and amygdala (Davidson, Putnam, & Larson, 2000).

A body of evidence shows that the orbitofrontal-insula, medial frontal anterior cingulate,and amygdala systems all interconnect with each other and with brain stem bioaminergic neu-romodulatory and hypothalamic neuroendocrine nuclei (see Figure 3). Although each has re-ciprocal connections with dopamine neurons in the ventral tegmental area of the anterior re-ticular formation and noradrenaline neurons of the caudal reticular formation, each limbicsubsystem maintains connections with different monoaminergic subnuclei (Halliday & Tork,1986; Halliday et al., 1988).

Because they are all components of the limbic system, each processes and imprints apositive or negative hedonic charge on current exteroceptive information about changes in theexternal social environment, and then integrates it with interoceptive information about con-current alterations in internal bodily states. Due to the facts that they each directly interconnectwith the ANS (Neafsey, 1990), and that autonomic activity is controlled by multiple integrativesites within the CNS that are heirarchically organized (Lane & Jennings, 1995), all are involvedin the regulation of bodily-driven affective states. Although all components process exterocep-tive and interoceptive information, the later maturing systems in the cortex will process thisinformation in a more complex fashion than the earlier subcortical components. The output ofthe lowest level limbic levels have the character of automatic innate reflexes, while higherprocessing produces more flexible intuitive responses that allow fine adjustment to environ-mental circumstances.

In optimal socio-emotional environments, each limbic level has bidirectional connectionswith the others, and in this manner information can both be forwarded up and down the limbicaxis for further appraisal and hierarchical modulation. The earliest and simplest appraisals ofexteroceptive and interoceptive affective stimuli would be hedonic and aversive affective coreprocesses in the amygdala (Berridge, 2000), the later and most complex subjective experiencesof pleasure and pain in the orbitofrontal areas (Blood, Zatorr, Bermudez, & Evans, 1999;Francis et al., 1999; Petrovic, Petersson, Ghatan, Stone-Elander, & Ingvar, 2000). These op-erations are primarily lateralized to the right limbic system, which is preferentially connecteddownward to the right neurochemical systems associated with emotion (Buck, 1994) and up-ward to the ipsilateral right neocortex (Wilson, Isokawa, Babb, Crandal, Levesque, & Engel,1991).

The concept of a hierarchically organized brain that develops through an increasinglycomplex coordination of lower and higher levels was first introduced by the British neurologistHughlings Jackson at the end of the nineteenth century. Jackson conceived of three levels oforganization, including the lowest and most primitive, middle, and last to evolve, highestcenters. Each of these levels is a representing system, with the highest level of integration andcoordination dependent upon prefrontal activity that allows the organism as a whole to adjustto the environment (Jackson, 1931). A similar trilevel model is also seen in MacLean’s (1990)triune brain. As applied to the developmental organization of the right limbic system of theright brain, this conception suggests a three-tiered self-organizing dynamic system. Increasedinterconnectivity (energy flow) among the three component circuits would allow for informa-


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FIGURE3.3.

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cap heightbase of texttion stored at one level to be transferred to the others. The top level that receives feedback

from the lower performs an executive function (Toates, 1998), and this allows for emergentproperties, that is, novel combinations of more complex emotional states.

In line with the Jacksonian ontogenetic concept of vertical brain organization (Luu &Tucker, 1996) and the principle of caudal-to-rostral brain development, amodel of the ontogenyof the limbic system can be offered. Keeping in mind that in humans this development continuespostnatally, reversing the sequence of the rostral limbic system (amygdala, anterior cingulate,insular-orbitofrontal) could offer specific ideas about how a number of discrete limbic com-ponents could come on line in a defined sequence in the first year. Recall Bowlby’s speculationthat the limbic system is centrally involved in attachment and that the “upgrading of controlduring individual development from simple to more sophisticated is no doubt in large part aresult of the growth of the central nervous system” (1969, p. 156).

The following sequence represents Bowlby’s “succession of increasingly sophisticatedsystems” that mediates attachment development. I further propose that the ontogenetic pro-gression of each of these limbic subsystems progresses from an initial sympathetic-dominantexcitatory phase followed by a latter parasympathetic-dominant inhibitory phase and ultimatelyexcitation-inhibition balance (see Schore, 1994).

At birth, only the amygdala (see Figure 2), a primitive limbic regulatory system thatappraises crude information about external stimuli and modulates autonomic and arousal sys-tems, is on line (Chugani, 1996). The right amygdala is known to be implicated in the pro-cessing of olfactory stimuli (Zald, Lee, Fluegel, & Pardo, 1998) within the mother and theperinatal infant relationship (Van Toller & Kendal-Reed, 1995). This suggests that right amyg-dala-driven processes underlie the infant’s recognition of the mother’s scent as well as themother’s recognition of neonates through olfactory cues (Porter, Cernoch, & McLaughlin,1983).

Amygdala memorial systems also mediate the organization of the earliest representationsof the infant maternal relationship that allow six-day-old infants to discriminate the scent oftheir mother’s breast pad (MacFarlane, 1977) or axillary odor (Cernoch & Porter, 1985) fromthat of another woman. This early appearing subcortical limbic control system is thus a centralcomponent of the proto-attachment mechanisms that are driven by the unique salience of ol-factory signals (Porter & Winberg, 1999). These data further suggest that dyadic “humanolfactory communication” (Russell, 1976) occurs between the mother’s and infant’s rightbrains. Limbic areas of the right hemisphere are also centrally involved in human gustation(Small et al., 1999).

The fact that the processing of olfactory/gustatory information is dominant in the perinatalperiod is also documented by developmental researchers. The primary organ of the body thatspecializes in the latter function is, of course, the mouth. According to Hernandez-Reif et al.(2000, p. 205):

The infant mouth, including the tongue, is a highly specialized multifunctional sensory-motor system designed to receive nutrients and to express discomfort, such as by variedcries that relay hunger or pain (van den Boom & Gravehurst, 1995). . . . Recent researchrevels that the newborn’s mouth is also a well-developed perceptual organ. Upon contactinga non-nutritive object, the tactile receptors of the mouth generate positive presssure, presum-ably for the purpose of detecting object information. (Butterworth & Hopkins, 1988; Rochat,1983)

These authors point out that newborns exhibit a transfer of learning from informationdetected by the mouth to other sensory modalities, citing studies which show that newborns

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cap heightbase of textsuck harder in order to see the visual (Walton, Bower, & Bower, 1992) and hear the auditory

stimulation (DeCasper & Fifer, 1980) emanating from the mother’s face. They also mentionthat at a later point of development (the second quarter of the first year; Morange-Majoux,Cougnot, & Bloch, 1997), exploration of objects shifts from the mouth to the hands(Bloch, 1998).

In the cerebral hemispheres only the primary somatosensory cortex is metabolically activeat birth (Chugani, 1996), and this area is known to process tactile and kinesthetic sensations.If the olfactory and gustatory systems are connecting into the amygdala prenatally, I suggestthat specifically somatosensory connections into the amygdala are also forming by the end ofthe first two months. Sufficient levels of tactile stimulation are provided by the maternal en-vironment in the form of maternal contact comfort that releases early protoattachment behavior.Taylor (1987) notes, “The sensations impinging on the infant’s skin presumably help regulateaspects of the infant’s behavior and physiology” (p. 164). In accord with this, the classicalwork of Harlow (1958) demonstrates that skin-to-skin contacts come on-line early, and thatthe infant actively seeks to adhere to as much skin surface on the mother’s body as possible.

Most human females cradle their infants on the left side of the body (Manning et al., 1997;Harris, Almergi, & Kirsch, 2000). This tendency is well developed in women but not in men,is independent of handedness, and is widespread in all cultures. It has been suggested that thisleft-cradling tendency “facilitates the flow of affective information from the infant via the leftear and eye to the center for emotional decoding, that is, the right hemisphere of the mother”(p. 327). It also has been observed that “the language of mother and infant consist of signalsproduced by the autonomic, involuntary nervous system in both parties” (Basch, 1976, p. 766).This hemisphere, deeply connected into the ANS, is specialized for tactile perception on bothsides of the body (Carmon & Benton, 1969) and for the perception and recall of spatial patternsof touch in nonverbal memory (Milner & Taylor, 1972). Again, the overt expressions of righthemisphere-to-right hemisphere communications are manifest from the very beginnings ofinfancy.

Neurobiological research indicates that “in early postnatal life, maintenance of criticallevels of tactile input of specific quality and emotional content is important for normal brainmaturation” (Martin, Spicer, Lewis, Gluck, & Cork, 1991, p. 3355). Indeed, the sensory inputderived from contact with the mother during nursing has been suggested to shape dendriticgrowth (Greenough & Black, 1992). Infantile handling, tactile stimulation associated withcomforting “holding” and “containing” experiences provided by themother, induces permanentmodifications of later hypothalamic CRF levels (Campbell, Zarrow, & Denenberg, 1973).Again, these experiences are right laterlized. Kalogeras et al. (1996) demonstrate that the rightside of the human hypothalamus is dominant for neuropeptide secretion, including CRF activity.

I further propose that areas of the amygdala in the medial temporal lobe, especially thecentral and medial nuclei, are in a critical period of maturation that onsets in the last trimesterof pregnancy and continues through the first two months of human life, the earliest period ofbonding. In growth-facilitating perinatal environments, the experience-dependent maturationof interconnections between the infant’s right amygdala and right paraventricular hypothalamicnuclei allow for coregulation of vasopressin and the antistress hormone oxytocin in early ma-ternal– infant interactions (Panksepp, 1998). This is a critical period of organization of theamygdalar–hypothalamic system, in which sensory information processed by the amygdalareceives a positive or negative hedonic charge and is then relayed to various hypothalamicnuclei (Fonberg, 1986). These events occur in what Bowlby (1969) calls the “preattachmentphase” of the first two months, the same time period of the evolution of Stern’s (1985) “emerg-ing self,” and the time-frame of the first-to-mature homeostatic control system described byBrazelton (2000) that is on-line in the first weeks of life.



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cap heightbase of textI previously cited a finding of a milestone for normal development in a rapid change in

brain maturation at eight weeks, reflecting the onset of a critical period during which synapticconnections in the primary visual cortex are modified by visual experience (Yamada et al.,1997, 2000). At this time infant visual preference behavior shifts from subcortical to corticalprocessing (Hoffmann, 1978), and face-to-face interactions, occurring within the primordialexperiences of human play, first appear (Cohn & Tronick, 1987). Fogel and Branco observe

Three-month old-infants signal their willingness to engage in play by both gazing at motherand smiling, and they use gaze away and the cessation of smiling or the onset of crying toindicate their desire to end a bout of play. Before three months, infants do not have theability to do this. (1997, p. 76)

In these play sequences of affective synchrony, dyadically amplified elevations in sym-pathetic arousal occur in gaze engagements, followed by infant increases in parasympatheticactivity (vagal nucleus ambiguus) in gaze aversion disengagements. The vagally controlledhormone, oxytocin, now is released by “sensory stimuli such as tone of voice and facial ex-pression conveying warmth and familiarity” (Uvnas-Molberg, 1997, p. 42). Vagal tone (Porges,1991) is undeveloped and weak in the first quarter of the first year, but increases significantlyat two to four months (Kagan, 1994), a time when primary intersubjectivity and delight andlaughter first appear (Sroufe, 1996).

This same interval represents the onset of a critical period for the development of theanterior cingulate areas (see Figure 2) of the medial frontal cortex, a region involved in playand separation behaviors, laughing and crying vocalizations, face representations, and modu-lation of autonomic activity (MacLean, 1993; MacLean & Newman, 1988; Paus, Petrides,Evans, & Meyer, 1993). MacLean (1987) provides evidence to show that this cortex is re-sponsible for vocalizations that “maintain maternal–offspring contact.” The anterior cingulateis also known to contribute to maternal behavior (Slotnick, 1967). A recent fMRI study revealsthat the mother’s cingulate and right orbitofrontal cortex respond to both pain and separationcries of an infant (Lorberbaum et al., 2000). With regard to the infant’s expanding capacities,the right cingulate and parietal areas have been implicated in exploratory attentionalmovements(Gitelman et al., 1996) in the generation of a subjective prediction, and in the anticipation ofbeing tickled (Carlsson, Petrovic, Skare, Petersson, & Ingvar, 2000).

Recall the earlier depiction of mutually regulated states of maternal– infant high arousal,attention, and vocalizations occuring in play experiences that emerge at this time (Feldman etal., 1999). This is also the onset of the positive resonances that occur within the mother– infant“protoconversations” that induce what Trevarthen calls primary intersubjectivity (Trevarthen,Aitken, Papoudi, & Roberts, 1998). In this relational context the primary caregiver’s anteriorcingulate-driven maternal behavior would be socially tuning the infant’s medial frontal cortex,thereby influencing the parcellation and final circuit wiring of the baby’s developing anteriorcingulate. During this critical period of the onset the infant’s anterior cingulate-right temporal(Nakamura et al., 2000) sulcus face processing, which Mahler et al. (1975) call the symbioticperiod, the infant forms a discriminate attachment to the mother’s face.

The later occurring parasympathetic phase of the critical period of growth of this limbiccomponent would occur in the third quarter, a time of cingulate-driven expressions of sepa-ration-anxiety (Joseph, 1992; MacLean, 1990), responses to attachment ruptures. At seven toten months infants show fear (Sroufe, 1996) and stranger anxiety, in which they inhibit ongoingbehavior and withdraw when exposed to novel and threatening situations and unfamiliar people.

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cap heightbase of textThe emergence of this more complex defensive behavior, inhibited approach, represents the

parasympathetic maturation of the cingulate.Furthermore, in light of the known role of the cingulate in consciousness (Kennard, 1955),

it is tempting to speculate that the experience-dependent maturation of this limbic structuremay be activated in moments of dyadically expanded states of consciousness that onset in themiddle of the first year. Tronick et al. (1998) are now describing how microregulatory social-emotional processes of communication literally expand intersubjective states of consciousnessin the infant–mother dyad. They argue that the baby’s self-organizing system, when coupledwith the mother’s, allows for a brain organization that can be expanded into more coherentand complex states of consciousness. The interpersonal context of a coregulated dyadic systemallows for “a mutual mapping of (some of) the elements of each partner’s state of consciousnessinto the other partner’s brain” (p. 296).

I suggest that Tronick is describing an expansion of what Edelman (1989) calls primaryconsciousness. Edelman states primary consciousness relates visceral and emotional informa-tion pertaining to the biological self to stored information pertaining to outside reality, and thatit is lateralized to the right brain. Activity of limbic cingulate areas are known to be associatedwith primary consciousness (Denton et al., 1999). This developmental work supports the ideathat consciousness is a product of that part of the brain that handles human relations, and is aproperty of a brain that is and has been in communication with other brains (Barlow, 1980;Schore, 1994). It also suggests that indices of the maturation of the infant’s capacity for primaryconsciousness needs to be included in our models of infant mental health.

The critical period of anterior cingulate-driven limbic maturation thus overlaps Bowlby’s(1969) phase of “attachment-in-the-making,” and mediates what Stern (1985) terms, “the coreself.” Brazelton (2000) describes the emergence in the second quarter of the first year of asecond homeostatic control system, one associated with a mutual reciprocal feedback system,although an advance of the former control system it is still “an immature psychophysiologicalsystem.” I suggest this system can be identified as a maturing anterior cingulate which nowhierarchically controls the earlier amygdala-dominated limbic configuration.

The right insula, a limbic structure involved in emotional and facial processing (Berthier,Starkstein, & Leiguarda, 1987), in integrating tonal structure with a speaker’s emotions andattitudes (Riecker, Ackermann, Widgruber, Dogil, & Grodd, 2000), and in visceral and auto-nomic functions that mediate the generation of an image of one’s physical state (Craig, Chen,Bandy, & Reiman, 2000) is also activated in primary consciousness (Denton et al., 1999). Thislimbic structure is implicated in pain processing and serves as an alarm center, “alerting theindividual to potentially distressing interoceptive stimuli, investing them with negative emo-tional significance” (Banzett, Mulnier, Murphy, Rosen, Wise, & Adams, 2000, p. 2120). It istempting to speculate that the experience-dependent maturation of this system is associatedwith both the more complex representation of body image and “stranger anxiety” that emergesin the second half year of life.

In the last quarter of the first year the quality of the infant’s social relatedness changesdramatically (see Schore, 1994), due to the concurrent rapid myelination and maturation ofdeveloping limbic and cortical association areas. If earlier face-to-face interactions contain onlyspontaneous communication processes, after nine months the infant can engage in “joint atten-tion,” the ability to shift attention between an object and a person. In this form of nonverbalcommunication the infant coordinates his visual attention with that of the caregiver, and is nownot only aware of an object but simultaneously aware of the mother’s attention to the object.In such instances of what Trevarthen et al. (1998) call “secondary intersubjectivity,” eachmember of the dyad coaligns separable, yet related forms of consciousness.

Joint attention occurs within highly affectively charged social referencing transactions, an



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cap heightbase of textattachment process that mediates a resonance of positive affect (Schore, 1994). This dyadic

mechanism allows the infant to appreciate that “the other person is a locus of psychologicalattitudes toward the world, that the other is ’attending’ in such a way that shared experiencesare possible” (Hobson, 1993, p. 267). In this manner the child comes to understand others “asintentional beings, that is, as subjects of experience possessing internal states such as interestand attention” (Tomasello & Camaioni, 1997, p. 20). To get an adult to tune into his attentionaland intentional focus on the world the infant now uses an expanded repertoire of bidirectionalcommunicative gestures, an important cognitive advance that communicates intention (Goldin-Meadow, 2000). It is also is in this period, the last quarter of the first year, when “the infantstarts to adopt a mentalistic strategy to interpret and predict the behavior of other agents” andis “capable of taking the intentional stance” (Gergely, Nadasdy, Csibra, & Biro, 1995, p. 184).In developmental neurobiological research, Caplan et al. suggest that “the development of jointattention might reflect maturation of the prefrontal cortex” (1993, p. 589).

These critical advances represent a further maturation of the right hemisphere, becausecurrent research suggests it contributes to attention and intention (Mattingley, 1999; Sturm etal., 1999). Very recent studies of joint attention demonstrate that the right (and not left) hemi-sphere shifts attention to where someone is looking to follow the gaze of another (Kingstone,Friesen, & Gazzaniga, 2000). In fact, there is now evidence for “a special role for the rightfrontal lobe in sustaining attention over time” (Rueckert & Grafman, 1996, p. 952). Very recentreports now reveal that the right orbitofrontal and right anterior insula cortices are componentsof a neural circuit that “enables integration of adaptive bodily responseswith ongoing emotionaland attentional states of the organism” (Critchley, Elliott, Mathias, & Dolan, 2000b, p. 3033).But in addition this right prefrontal cortex is fundamentally involved in “regulating emotionalresponses” (Hariri, Bookheimer, & Mazziotta, 2000).

THE MATURATION OF AN ORBITOFRONTALREGULATORY SYSTEM

In Affect Regulation and the Origin of the Selfand continuing works I offer evidence to showthat the orbital prefrontal cortex enters a critical period of growth that spans the last quarter ofthe first through the middle of the second year, an interval that corresponds with the beginningsof human socialization. The critical period of orbitofrontal-driven limbic maturation thus over-laps and mediates what Stern (1985) terms the developmental achievement of “the subjectiveself.” This prefrontal limbic structure is reciprocally interconnected with other limbic areas inthe insula (Augustine, 1996), anterior cingulate (Devinsky et al., 1995), and the amygdala(Barbas & de Olmos, 1990), and represents the hierarchical apex of the limbic system.

Brothers (1995, 1997) describes a limbic circuit of orbitofrontal cortex, anterior cingulategyrus, amygdala, and temporal pole which functions as a social “editor” that is “specializedfor processing others’ social intentions” by appraising “significant gestures and expressions”(Brothers, 1997, p. 27) and “encourages the rest of the brain to report on features of the socialenvironment” (p. 15). The editor acts as a unitary system “specialized for responding to socialsignals of all kinds, a system that would ultimately construct representations of the mind” (p.27). Mesulam points out that the prefrontal areas involved in emotional modulation and atten-tional functions help to create “a highly edited subjective version of the world” (1998, p. 1013).This emergent subjective function is the outcome of a secure attachment.

In a recent entire issue ofCerebral Cortexon “The mysterious orbitofrontal cortex,” theeditors conclude that “the orbitofrontal cortex is involved in critical human functions, such associal adjustment and the control of mood, drive and responsibility, traits that are crucial indefining the ’personality’ of an individual” (Cavada & Schultz, 2000, p. 205). Referring back

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FIGURE 4.4. Relationships of the orbitofrontal cortex to subcortical structures of the right hemisphere(from Smith, 1981).

to Brazelton and Cramer’s conception of the developmental reorganization of control systems,neurobiological studies show that the mature orbitofrontal cortex acts in “the highest level ofcontrol of behavior, especially in relation to emotion” (Price, Carmichael, & Drevets, 1996, p.523). This prefrontal system, which functions in “emotional control” (Roberts & Wallis, 2000)and acts to “control autonomic responses associated with emotional events” (Cavada,Company,Tejedor, Cruz-Rizzolo, & Reinoso-Suarez-Suarez, 2000) is identical to Bowlby’s control sys-tem of attachment (see Figure 4; for a further characterization of this prefrontal system, seeSchore 1994, 1996, 1997a, 1997b, 1998a, 1998b, 1999a, 2000 b, 2000d, in press a, in press b).

This control system integrates the psychological and biological spheres of mind and body.The orbitofrontal cortex is known to play an essential role in the processing of interpersonalsignals necessary for the initiation of social interactions between individuals (Schore, 1994).This cortex, along with the superior temporal sulcus and amygdala, comprises a circuit thatmediates social gaze (Emery, 2000). Orbitofrontal neurons specifically process visual and au-ditory information associated with emotionally expressive faces and voices (Scalaidhe,Wilson,Goldman-Rakic, 1997; Romanski, Tian, Fritz, Mishkin, Goldman-Rakic, 1999). But this fron-tolimbic system is also involved in the representation of highly integrated information on theorganismic state (Tucker, 1992). The systems that biochemically regulate all brain and bodilystate phenomena are located in discrete groups of arousal-regulating bioaminergic neurons ofthe subcortical reticular formation that innervate wide areas of the brain through diffuse pro-jections (Lydic, 1987). It now thought that the most basic level of regulatory process is theregulation of arousal (Tucker, Luu, & Pribram, 1995). The orbitofrontal cortex, especially in



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cap heightbase of textthe right hemisphere, “is involved in “both generation and afferent feedback representation of

arousal” (Critchley et al., 2000b, p. 3037).This prefrontal area regulates dopaminergic arousal (Iversen, 1977) via its direct reciprocal

connections with dopamine neurons in the ventral tegmental area of the anterior reticular for-mation. It also projects to the ventral striatum and the core of the nucleus accumbens, a basalganglia structure innervated by dopamine neurons and centrally involved in motivated behavior(Haber, Kunishio, Mizobuchi, & Lynd-Balta, 1995; Mogenson, Jones, & Yim, 1980), in thenonverbal decoding of positive facial expressions (Morris, Robinson, Raphael, & Hopwood,1996), and in mechanisms of pleasant reward and motivation (Robbins & Everitt, 1996). Theright nucleus accumbens (and the right cingulate) are activated in the encoding of pleasantemotional stimuli (Hamann, Ely, Graffton, Kilts, 1998).

This excitatory limbic circuit, the ventral tegmental limbic forebrain–midbrain circuit(Schore, 1994, 1996), is involved with the generation of positively valenced states associatedwith approach behavior, motivational reward, and active coping strategies. Recent neuroim-aging data indicates that the lateral orbital prefrontal areas (which is irrigated by the middlecerebral artery) are specialized for regulating excitement (Elliot, Dolan, & Frith, 2000) andother positive emotional states (Northoff et al., 2000). Midbrain dopamine neurons are knownto be preferentially activated by positively valenced appetitive rather than negatively valencedaversive stimuli (Mirenowicz & Schultz, 1996), and to exert an inhibitory influence on cortisolreceptors (Casolini et al., 1993).

Phasic increases in dopamine activity allow the individual to immediately appraise thesalience of biologically important stimuli in the environment (Berridge & Robinson, 1998). Itis important to note, however, that there is an optimal range of stimulation of the dopamine(D1) receptor that mediates working memory in the prefrontal cortex (Williams & Goldman-Rakic, 1995), and that dopamine levels that are either too low or too high impair its functionaloutput (Arnstein & Goldman-Rakic, 1998; Zahrt, Taylor, Mathews, & Arnsten, 1997). Optimalactivation of the ventral tegmental limbic forebrain–midbrain circuit is described not by alinear function but by an inverted “U” relationship. I suggest that an individual’s unique narrowor broad optimal orbitofrontal ventral tegmental dopaminergic profile is set up during its criticalperiod of development in positively valenced attachment transactions.

Orbitofrontal regions also have reciprocal connections with arousal-regulating noradre-nergic neurons in the medulla oblongata solitary nucleus and the vagal complex in the brainstem caudal reticular formation, and onto subcortical targets in parasympathetic autonomicareas of the lateral hypothalamus, thereby completing the organization of another latermaturinglimbic circuit, the lateral tegmental limbic forebrain–midbrain circuit that activates the onsetof an inhibitory state, regulates negative affect, and is associated with avoidance and passivecoping (see Schore, 1994, 1996). Orbital-amygdala interactions allow the individual “to avoidmaking choices associated with adverse outcomes, without their first having to experience theseadverse conditions” (Baxter, Parker, Lindner, Izquierdo, &Murray, 2000, p. 4317). Stimulationof orbitofrontal noradrenergic inhibitory circuits results in “behavioral calming” (Arnsten,Steere, & Hunt, 1996). Optimal activity is also described by an inverted “U” relationship, oneorganized in critical period attachment transactions of interactive repair of negative states.Neuroimaging studies show the medial orbitofrontal areas (irrigated by the anterior cerebralartery) are specialized for processing negative emotional states (Northoff et al., 2000; Paradiso,Chemerinski, Vazici, Tartaro, & Robinson, 2000).

The functioning of the two limbic circuits (see Figure 3) underlies the observation thatemotions organize behavior along a basic appetitive-aversive dimension associated with eithera behavioral set involving approach and attachment, or a set disposing avoidance, escape, anddefense (see Schore, 1994, 1996, 1997b). A number of theorists have suggested that positive

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cap heightbase of textand negative affect are mediated by different neural circuitries (e.g., Gray, 1990; Cacioppo &

Berntson, 1994), and very recent neuroimaging data demonstrate that the neural activationpattern of happiness is “remarkably distinct” from sadness (Damasio et al., 2000).

The orbitofrontal system has been termed the “Senior Executive of limbic arousal” (Joseph,1996). This is due to the fact that it has reciprocal connections with both dopaminergic neuronsin the ventral tegmental area of the anterior reticular formation, aswell as noradrenergic neuronsin the solitary tract of the medullary areas of the caudal reticular formation (and serotoninneurons in the raphe nucleus). In the orbitofrontal areas dopamine excites and noradrenalineinhibits neuronal activity (Aou, Oomura, Nishino, Inokucki, & Mizuno, 1983). These opposingmechanisms of excitation and inhibition provide for rapid regulation of gradedmetabolic outputand thereby functional activity. Subtle external perturbations would trigger changes in thiscontrol parameter, preferentially activating the excitatory lateral orbitofrontal subsystem andits connections into dopamine neurons that modulate large area of the brain and/or the inhibitorymedial orbitofrontal subsystem and its connections into noradrenaline neurons that also inner-vate widely separated brain regions (Foote, 1987). In this manner small changes in the exci-tation-inhibition balance of the dual orbitofrontal system lead to large changes in the activityof state-regulating neuromodulators that regulate far-reaching neural networks.

The structural connections within and between the lateral and medial orbitofrontal sub-systems and the excitation-inhibition balance between them are a product of both genetic andenvironmental factors, specifically the caregiver’s attachment function as a regulator of theinfant’s arousal. Bowlby (1969) speculated that the functions of the attachment control systemare associated with the organism’s “state of arousal” that results from the critical operations ofthe reticular formation, and with “the appraisal of organismic states and situations of the mid-brain nuclei and limbic system” (1969, p. 110).

Furthermore, due to the interconnections of the orbitofrontal system into the cervical,thoracic, lumbar, and sacral divisions of the spinal cord (Burstein & Potrebic, 1993) and intothe vagal nerve that delivers autonomic information, it receives (like the amygdala and anteriorcingulate) moment-to-moment interoceptive information from the entire body, especially in-formation concerning changes in autonomic arousal and in bodily or “somatic” states. Becauseof its intimate connections with the hypothalamus (Ongur, An, & Price, 1998), the head gan-glion of the ANS and the brain’s major control center for energy expenditure (Levin & Routh,1996), the orbital prefrontal area acts as a major center of CNS hierarchical control over theenergy-expending sympathetic and energy-conserving parasympathetic branches of the ANS.The ANS is responsible for the somatic aspects of all affective states. In optimal early envi-ronments, a system emerges in which higher brain areas can modulate a flexible coping patternof coupled reciprocal autonomic control, in which increases in one ANS division are associatedwith decreases in the other (Berntson, Cacioppo, & Quigley, 1991).

This frontolimbic system is particularly involved in situations in which internally generatedaffective representations play a critical role (Zald & Kim, 1996), and in the implicit processing(Critchley et al., 2000a; Rolls, 1996) and procedural learning (de Guise, del Pesce, Foschi,Quattrini, Papo, & Lussonde, 1999) of socioemotional information. The orbitofrontal systemis now described as “a nodal cortical region that is important in assembling and monitoringrelevant past and current experiences, including their affective and social values” (Cavada etal., 2000, p. 238). Orbitofrontal neurons are specialized for working memory, a sequentialprocessing of information in real time, i.e., on a moment-to-moment basis (Goldman-Rakic,Muly, & Williams, 2000). These procedures include encoding a facially expressed affectivestimulus, maintaining it “on-line,” and directing an adaptive memory-guided response. As aresult of such operations the orbitofrontal cortex is centrally involved in “acquiring very specificforms of knowledge for regulating interpersonal and social behavior” (Dolan, 1999, p. 928).



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cap heightbase of textThere is now evidence that the right inferior frontal regions mediate nonverbal memorial

encoding and retrieval (Wagner, Poldrack, Eldridge, Desmond, Glover, & Gabrieli, 1998). Theoperations of the right orbitofrontal control system involve a rapid subcortical evaluation ofthe regulatory significance of an external environmental stimulus, a processing of feedbackinformation about the current internal state to make assessments of coping resources, and anadaptive updating of context-appropriate autonomic response outputs to make adaptive ad-justments to particular environmental perturbations (Schore, 1998a). In this manner the orbi-tofrontal areas are involved in the regulation of autonomic responses to social stimuli (Zald &Kim, 1996), the spontaneous gut feelings to others.

The orbitofrontal cortex is situated at the hierarchical apex of an “anterior limbic prefrontalnetwork” that interconnects it with the temporal pole, cingulate, and amygdala, and throughthese linkages it plays an essential role in affect regulation (Davidson et al., 2000; Schore,1994). The early maturing amygdala acts as a sensory gateway to the limbic system, butamygdala processing, although very rapid, is crude compared to the more complex processingof affective stimuli by later maturing corticolimbic areas. A recent fMRI study (Teasdale etal., 1999) demonstrates that while the subcortical amygdala responds to emotional stimuli at adirect perceptual level, its operations are less relevant to cognitively elicited emotions. Incontrast, the ventromedial cortex is known as “the thinking part of the emotional brain.” Inoptimal contexts the orbitofrontal cortex takes over amygdala functions (Rolls, 1996), and“provides a higher level coding that more flexibly coordinates exteroceptive and interoceptivedomains and functions to correct responses as conditions change” (Derryberry & Tucker,1992, p. 335).

Operating at levels beneath awareness, it is activated “when there is insufficient infor-mation available to determine the appropriate course of action” (Elliott, Dolan, & Frith, 2000,p. 308), but subsequently this regulatory system monitors, adjusts, and corrects emotionalresponses and regulates the motivational control of goal-directed behavior. It thus functions asa recovery mechanism that efficiently monitors and regulates the duration, frequency, andintensity of positive and negative affect states, from high intensity joy and excitement (Schore,1994) to the affective-motivational aspects of pain (Gyulai, Firestone, Mintun, &Winter, 1997;Petrovic et al., 2000).

The functioning of this system thus allows for “the emotional modulation of experience”(Mesulam, 1998). Orbitofrontal areas function to “integrate and assign emotional-motivationalsignificance to cognitive impressions; the association of emotion with ideas and thoughts”(Joseph, 1996, p. 427) and in “the processing of affect-related meanings” (Teasdale et al.,1999). A recent neuropsychological study indicates that the orbitofrontal cortex is “particularlyinvolved in generating a theory of mind tasks with an affective component” (Stone, Baron-Cohen, & Knight, 1998, p. 651). These adaptive capacities are the outcome of a secure attach-ment.

The orbitofrontal system is specialized to act in contexts of “uncertainty or unpredictabil-ity” (Elliott et al., 2000, p. 308), an operational definition of stress. Its functions mediateaffective shifts, the alteration of behavior in response to fluctuations in the emotional signifi-cance of stimuli (Dias, Robbins, & Roberts, 1996). In optimal frontolimbic operations, theseshifts from one emotional state to another are are experienced as rhythms in feeling states andare fluid and smooth, a flexible capacity of a coherent dynamic system. Efficient orbitofrontaloperations organize the expression of a regulated emotional response and an appropriate mo-tivational state for a particular social environmental context, and in this fashion it contributesto “judicious, adapted behavior” (Cavada et al., 2000). These coping capacities define an ef-ficient limbic system, the brain network responsible for the organization of new learning andthe capacity to adapt to a rapidly changing environment. The right limbic system is centrally

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cap heightbase of textinvolved in complex attachment functions and interpersonal coping strategies, and its opera-

tions are instrumental to adaptive infant mental health.The efficient functioning of this frontolimbic cortex is thus manifest in its capacity to

mediate between the external environment and the internal milieu. At 18 months, the time oforbitofrontal maturation, toddlers have been observed to have a “vastly enhanced capacity forexperiencing the internal milieu” (Greenspan, 1979). Lieberman has emphasized that, “in thelast two decades . . . efforts at understanding the subjective world of the infant have focusedprimarily on mental representations as the building blocks of inner experience. The baby’sbody, with its pleasures and struggles, has largely been missing from this picture” (1996, p.289). These findings suggest that bodily intactness, somatic and physical functioning, mecha-nisms for coping with illness and pain, and general psychobiological integrity need to beincluded in operational definitions of infant mental health.

REGULATORY FUNCTIONS OF THE RIGHT BRAIN

The orbital prefrontal region, the “Senior Executive” of the social-emotional brain (Joseph,1996), is especially expanded in the right cortex (Falk, Hildebolt, Cheverud, Vannier, He-lmkamp, & Konigsberg, 1990), and, indeed, it comes to act in the capacity of an executivecontrol function for the entire right brain. Because the early maturing and “primitive” rightcortical hemisphere contains extensive reciprocal connections with limbic and subcorticalregions (Tucker, 1992), it is dominant for the processing and expression of emotional infor-mation (Schore, 1994, 1999a, 2000a, in press a). The extensive reciprocal right frontal-sub-cortical connections, especially with bioaminergic and hypothalamic subcortical nuclei, accountfor the unique contribution of this hemisphere in regulating homeostasis and modulating phys-iological state in response to internal and external feedback.

It has been known for some time that arousal systems are right-lateralized (Heilman &Van Den Abell, 1979), and now there is data to show that the hypothalamus, the core brainsystem where hormonal control and visceral-emotional reactions are regulated (Kupferman,1985), is also right-lateralized (Kalogeras et al., 1996). MRI research reveals that the rightanterior temporal lobe is larger than the left from early infancy (Utsunomiya, Takano, Okazaki,& Mitsudome, 1999), and that the diencephalic hypothalamic nuclei are considerably largeron the right side of the human brain (Sowell & Jernigan, 1998). The right hemisphere, moreso than the left, is deeply connected into the ANS (Erciyas, Topalkara, Topaktas, Akyuz, &Dener, 1999; Lane & Jennings, 1995; Yoon, Morillo, Cechetto, & Hachinski, 1997), and sothe representation of interoceptive information, the dynamic flows of visceral and somaticstates, is under primary control of this hemisphere.

But this hemisphere is also specialized for processing significant patterns of exteroceptiveinformation. The right hemisphere is faster than the left in performing valence-dependent,automatic, preattentive appraisals of emotional facial expressions (Pizzagalli, Regard, & Leh-mann, 1999) and in assessing visual or auditory emotional communicative signals (Nakamuraet al., 1999). The right cortex is responsive to not only the positive aspects of facial expressions(Blair, Morris, Frith, Perrett, & Dolan, 1999), visual stimuli (Muller, Keil, Gruber, & Elbert,1999), touch, smell (Francis et al., 1999), and music (Blood et al., 1999), but also for thenegative emotional/motivational aspects of pain (Hsieh, Belfrage, Stone-Elander, Hansson, &Ingvar, 1995; Hari, Portin, Kettenmann, Jousmaki, & Kobal, 1997). In fact, this hemisphereplays an essential role in the nonconscious appraisal of the positive or negative emotionalsignificance of social stimuli via a mechanism similar to Freud’s pleasure–unpleasureprinciple(Schore, 1998a, 1998c, 1999a, 1999c, in press b). These findings are not consonant with earliermodels that held that positive approach-related emotions are lateralized to the left hemisphere



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cap heightbase of textand negative withdrawal-related emotions to the right (Davidson, Ekman, Saron, Senulis, &

Friesen, 1990), a position not supported by recent brain imaging techniques (Canli, 1999).Citing only one example, Damasio’s group (2000) reports a PET study revealing that happinessis associated with activation of the right orbitofrontal right indula, right somatosensory, rightanterior cingulate, and right hypothalamus.

The coprocessing of exteroceptive and interoceptive information is possible when thehigher cortical limbic regions of the right hemisphere are actively and bidirectionally com-municating with the different levels of the right subcortical limbic regions. This organizationalmode allows for the operation of right-lateralized (dual) circuit of emotion regulation that isinvolved in “intense emotional-homeostatic processes” and in the modulation of “primary”emotions (Porges, Doussard-Roosevelt, & Maiti, 1994). These authors describe a vagal circuitof emotion regulation lateralized on the right side of the brain.

Vagal tone is defined as “the amount of inhibitory influence on the heart by the parasym-pathetic nervous system” (Field, Pickens, Fox, Nawrocki, & Gonzalez, 1995, p. 227), andalthough it is present at birth, it evolves in an experience-dependent manner over the first twoyears. A functional progression in vagal tone occurs from the middle of the first to the middleof the second year (Sweet, McGrath, & Symons, 1999). The progressive postnatal assemblyof this limbic–autonomic circuit (Rinaman et al., 2000) is reflected in a developmental shiftfrom interactive regulation to autoregulation of negative affective states. This ontogeneticachievement represents the evolution, at 18 months, of the right lateralized orbitofrontal-dom-inated lateral tegmental limbic forebrain–midbrain parasympathetic inhibitory circuit.

Current studies indicate that “right hemisphere control exists over both parasympatheticand sympathetic responses” (Spence et al., 1996, p. 118), the autonomic somatic componentsof all emotional states. For the rest of the lifespan the right brain plays a superior role in theregulation of fundamental physiological and endocrinological functions whose primary controlcenters are located in subcortical regions of the brain. There is also now evidence to show thatthe right hemisphere is dominant for the production of cortisol (Wittling & Pfluger, 1990),CRF and ACTH (Kalogeras et al., 1996), and indeed for immune, neuroendocrine, and cardio-vascular functions (Hugdahl, 1995; Sullivan & Gratton, 1999).

Because the hypothalamo–pituitary–adrenocortical axis and the sympathetic–adreno-medullary axis that mediate coping capacities are both under the main control of the rightcerebral cortex, this hemisphere contains “a unique response system preparing the organism todeal efficiently with external challenges,” and so its adaptive functions mediate the humanstress response (Wittling, 1997, p. 55). It, therefore, is centrally involved in the vital functionsthat support survival and enable the organism to cope actively and passively with stress. Theattachment relationship thus directly shapes the maturation of the infant’s right brain stress-coping systems that act at levels beneath awareness. In line with Bowlby’s description of a“control system” that regulates attachment behavior, the right hemisphere is dominant for“inhibitory control” (Garavan, Ross, & Stein, 1999).

Furthermore, the right brain stores an internal workingmodel of the attachment relationshipwhich encodes strategies of affect regulation that maintain basic regulation and positive affecteven in the face of environmental challenge (Schore, 1994). Because this hemisphere is cen-trally involved in unconscious processes (Joseph, 1992b; Schore, 1998c, 1999a, in press a, inpress b) and in “implicit learning” (Hugdahl, 1995), nonconsciously processed socio-emotionalinformation is stored in right cerebral implicit-procedural memory. Neuropsychological studiesreveal that this hemisphere, and not the later forming verbal– linguistic left, is the substrate ofautobiographical memory (Fink, Markowitsch, Reinkemeier, Bruckbauer, Kessler, & Heiss,1996).

Continuing these ideas, I suggest that the expansion of the earlier maturing ventral stream

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cap heightbase of text(Ungerleider & Haxby, 1994) in the right hemisphere accounts for its role in “implicit,” or

“procedural” learning, while the predominance of the later maturing dorsal stream in the leftunderlies its emphasis in “explicit” or “declarative” functions. Zaidel, Esiri, and Beardsworth’s(1998, p. 1050) proposal that “human memory systems in the two sides are wired up differentlyto support separate but complementary functional specialization in the hemispheres” suggeststhat the storage of right hemispheric implicit-procedural learning (Hugdahl, 1995) of affectiveinformation may be mediated by very different operations than explicit learning and memorialsystems of the left (Gabrieli, Poldrack, & Desmond, 1998).

The right hemisphere contributes to the development of reciprocal interactions within themother– infant regulatory system (Taylor, 1987), and mediates the capacity for biological syn-chronicity, the regulatory mechanism of attachment. In further support of its role in organismicsynchronicity, the activity of this hemisphere is instrumental to the empathic perception of theemotional states of other human beings (Schore, 1994, 1999a, in press, a). The right hemispheredecodes emotional stimuli by “actual felt [somatic] emotional reactions to the stimuli, that is,by a form of empathic responding” (Day & Wong, 1996, p. 651). According to Adolphs,Damasio, Tanel, Cooper, & Damasio, “recognizing emotions from visually presented facialexpressions requires right somatosensory cortices,” and in this manner “we recognize anotherindividual’s emotional state by internally generating somatosensory representations that stim-ulate how the individual would feel when displaying a certain facial expression” (2000, p.2683). The interactive regulation of right brain neuropsychology and attachment psychobiologyis thus the substrate of empathy, another fundamental aspect of adaptive infant metal health.

CONTINUED ORBITOFRONTAL AND RIGHT BRAINDEVELOPMENT AND ADAPTIVE MENTAL HEALTH

The orbital cortex matures in the middle of the second year, a time when the average child hasa productive vocabulary of less than 70 words. The core of the self is thus nonverbal andunconscious, and it lies in patterns of affect regulation. This structural development allows foran internal sense of security and resilience that comes from the intuitive knowledge that onecan regulate the flows and shifts of one’s bodily-based emotional states either by one’s owncoping capacities or within a relationship with caring others. As a result of developmentalneurobiological studies, Ryan and colleagues (1997) conclude that the operation of the rightprefrontal cortex is integral to autonomous regulation, and that the activation of this systemfacilitates increases in positive affect in response to optimally challenging or personally mean-ingful situations, or decreases in negative affect in response to stressful events.

The activities of the “self-correcting” orbitofrontal system are central to self-regulation,the ability to flexibly regulate emotional states through interactions with other humans—in-teractive regulation in interconnected contexts via a two-person psychology, and without otherhumans—autoregulation in autonomous contexts via a one-person psychology. As Sander(1997) notes, in health both poles are primarily suffused with positive affects. The adaptivecapacity to shift between these dual regulatory modes, depending upon the social context,emerges out of a history of secure attachment interactions of a maturing biological organismand an attuned social environment. The essential aspect of this function is highlighted byWesten,who asserts that “The attempt to regulate affect—to minimize unpleasant feelings andto maximize pleasant ones—is the driving force in human motivation” (1997, p. 542). Theefficient functioning of the orbitofrontal system is thus necessary for adaptive infant (and adult)mental health.

But this system is also necessary for later mental health. In a recent issue of theAmericanPsychologist, Bargh and Chartrand assert,



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cap heightbase of textmost of moment-to-moment psychological life must occur through nonconscious means if

it is to occur at all . . . various nonconscious mental systems perform the lion’s share ofthe self-regulatory burden, beneficiently keeping the individual grounded in his or her currentenvironment. (1999, p. 462)

These regulatory mental systems care are not innate, but a product of the experience-dependentmaturation of the orbitofrontal system that generates nonconscious biases that guide behaviorbefore conscious knowledge does (Bechara, Damasio, Tanel, & Damasio, 1997). Such non-conscious regulatory mechanisms are embedded in implicit-procedural memory in unconsciousinternal working models of the attachment relationship that encode strategies of affect regu-lation. The orbitofrontal cortex is involved in procedural learning (de Guise et al., 1999), andthe right cerebral hemisphere is dominant for implicit learning (Hugdahl, 1995), and so at allpoints of the lifespan this “Senior Executive of the social-emotional brain” is centrally involvedin “emotion-related learning” (Rolls, Hornak, Wade, & McGrath, 1994). Current definitions ofintuition as “the subjective experience associated with the we of knowledge gained throughimplicit learning” (Lieberman, 2000, p. 109) clearly suggest that intuitive thinking is a rightbrain process.

Implicit learning is also a major mechanism for the incorporation of cultural learning, aprocess that initiates in infancy. Tucker (1992) asserts that social interaction that promotesbrain differentiation is the mechanism for teaching “the epigenetic patterns of culture,” andthat successful social development requires a high degree of skill in negotiating emotionalcommunication, “much of which is nonverbal.” He also states that the important brain systemsin such functions are those that are involved in affective communication processes andmediatesocialization. Tucker concludes that such emotional information engages specialized neuralnetworks in humans, within the right hemisphere. Socialization is essential to advances inemotional–motivational development and to expansion of the self. A recent neuropsycholog-ical study concludes that “self-related material is processed in the right hemisphere” (Keenan,McCutcheon, Freund, Gallup, Sanders, & Pascual-Leone, 1999, p. 1424).

The right hemisphere subsequently reenters into growth spurts (Thatcher, 1994) and ulti-mately forms an interactive system with the later maturing left (Schore, 1994; Siegel, 1999).This structural attainment, at 15 to 30 months, allows for the emergence of what Stern (1985)calls “the verbal self.” The term “verbal self ” connotes a purely left brain mechanism, and yetit may really be an emergent function of an early maturing and expanding right brain and itconnections into the later maturing left.

In describing a model of lingusitic development, Locke proposes

The first phase is indexical and affective; the infant is strongly oriented to the human faceand voice, and learns caregivers’ superficial characteristics. The second phase is primarilyaffective and social: its function is to collect utterances, a resposibility that is subservedlargely by mechanisms of social cognition sited primarily in the right hemisphere. (1997,pp. 265–266)

Thus, both the first stage, which spans the last trimester of pregnancy to five to seven months,and the second, which continues to 20–37 months, are heavily driven by the right hemisphere.Although the left hemisphere begins a growth spurt at around 18 months, the right hemisphereis dominant through 36 months (Chiron et al., 1997).

Indeed, despite a pervasive tendency for scientists and clinicians to automatically assumethat language involves operations solely of the left hemisphere, there is now a growing body

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points in the lifespan for processing prosodic information in infants (Snow, 2000), children(Cohen, Branch, & Hynd, 1994), and adults (George et al., 1996; Schmitt, Hartje, & Willmes,1997), for comprehension of language (Beeman & Chiarello, 1998), lexical emotional stimuli(Cicero et al., 1999), and communicative pragmatics (Van Lancker, 1997), and for emotional(Blonder et al., 1991) communication.

Current neurobiological studies indicate that “while the left hemisphere mediates mostlinguistic behaviors, the right hemisphere is important for broader aspects of communication”(Van Lancker & Cummings, 1999, p. 95). Buck notes that “language is not simply a matter of‘cold cognition’: strong motivational and emotional forces invigorate the learning of languageand infuse its application with intensity and energy,” and emphasizes the adaptive nature ofright hemispheric “spontaneous emotional communication” (1994, p. 266). At all points of thelifespan nonverbal and verbal spontaneous emotional communications are outputs of the rightbrain attachment system.

It is important to point out that these communications are positively and negatively val-enced, and so in addition to “satisfying” the attachment system, they can also stress it. In otherwords, they are also sources of interpersonal stressors and stress regulation, processes that tapdirectly into the unique functions of the right brain. Scherer (1994) describes facially andvocally expressed “highly emotionally charged affect bursts” associated with activation of theANS. These events, although lasting for very brief periods, accommodate the needs of infor-mation processing and behavioral adaptation:

One of the fundamental characteristics of an emotional episode . . . is thesynchronizationof the different components in the organism’s efforts to recruit as much energy as possibleto master a major crisis situation (in a positive or negative sense). (p. 186)

I suggest that this principle applies to the developmental crises that must be mastered asone moves along the lifespan. The continuing growth spurts of the right hemisphere (Thatcher,1997) that mediates attachment, the synchronization of right brain activities between andwithinorganisms, thus occur as the developing individual is presented with the stresses that are in-trinsic to later stages of life, childhood, adolescence, and adulthood (Erikson, 1950; Seligman& Shahmoon-Shanok, 1995). The expanding ability of the individual to cope with interpersonaland bodily stressors is an important achievement in continuing human development, and itrepresents an expansion of the right brain, the hemisphere dominant for the human stressresponse. In terms of interpersonal stressors, this hemisphere is specialized for processing notonly facially expressed auditory (Snow, 2000) but also visual emotional information in infants(de Schonen et al., 1993), children (de Haan, Nelson, Gunnar, & Tout, 1998), and adults (Kimet al., 1999). These right brain capacities are essential to all interactions between humans,including the social bonding between “companions” (Trevarthen, 2000). Panksepp (2000),notes that “the underlying neurobiological mechanisms for bonding are quite similar to thosethat sustain the affective side of friendships.” Such interpersonal experiences facilitate futuregrowth of the brain and therefore personality.

Attachment theory is fundamentally a theory of the development of the personality overthe lifespan (Ainsworth & Bowlby, 1991). Weinfeld, Sroufe, Egeland, and Carlson (1999) offera number of possible explanations for why early attachment experiences influence developmentat later stages of life: the early attachment relationship may serve as a foundation for learningaffect regulation; it may influence subsequent development through behavioral regulation andbehavioral synchrony; or through the continuing presence, over the course of the ensuing



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cap heightbase of textdevelopmental trajectory, of early forming internal representations. But these authors offer one

other mechanism:

[I]t is possible that the experiences within the early attachment relationship influence thedeveloping brain, resulting in lasting influences at a neuronal level (Schore, 1994). Thispossibility . . . (is) compelling. (Weinfeld et al., 1999, p. 75)

In parallel writings in the neuroscience literature on the concept of development, Pandya andBarnes (1987, p. 66) assert the principle that:

Each stage in development is marked by a more differentiated cytoarchitecture and a newset of connections, which together might reasonably be expected to subserve a new, andmore advanced, behavior.

Thatcher (1994, 1997) has provided evidence to show that the right hemisphere, especially itsfrontal areas, continues subsequent growth spurts. I suggest that the ongoing maturationalpotential of an individual right brain is related to its attachment-influenced early organization,and that as in infancy, this further growth of right-lateralized cortical–subcortical systems isexperience dependent.

For example, as the toddler becomes a young child, age-appropriate interactions with peersdepend upon an efficient right hemispheric ability to engage in processes of affective synchronywith other children. This capacity involves the abilities to nonconsciously yet efficiently readfaces and tones, and therefore, the intentionalities of peers and teachers, to empathically res-onate with the states of others, to communicate emotional states and regulate interpersonalaffects, and thus to cope with the novel ambient interpersonal stressors of early childhood. Inlight of the fact that both the right and left hemispheres enter into subsequent growth spurtsfrom ages four through ten and that the frontal lobes continue to reorganize (Thatcher, 1997),the cognitive–emotional advances of late childhood reflect more complex connections withinthe right and between the emotional right and verbal– lingusitic left hemisphere.

In a recent chapter on attachment in adolescence, Allen and Land (1999) offer sections on“continuity in the meaning and status of attachment from infancy through adolescence” andon “emotion-regulating functions of adolescent attachment organization.” In parallel writingsin neuroscience, Spear (2000) presents a rapidly growing body of studies to show that the brainundergoes a significant reorganization during adolescence, and that this maturation contributesto the multiple psychological changes seen at this time of transition between childhood andadulthood. She notes, “adolescence is second only to the neonatal period in terms of both rapidbiopsychosocial growth as well as changing environmental characteristics and demands” (p.428), and that after a relatively long period of slowed growth during early childhood, theadolescent brain undergoes a prominent developmental transformation.

Indeed, overproduction and pruning of synapses, as in the postnatal period, is a hallmarkof adolescence (Huttenlocher, 1984). It has been estimated that 30,000 synapses are lost persecond in the primate cortex over the adolescent period, resulting in an ultimate reduction ofalmost one-half of the number of synapses per neuron in the preadolescent period (Rakic,Bourgeois, & Goldman-Rakic, 1994). During this time, as in human infancy, hypothalamic-regulated gonadal hormones reach very high levels, and Spear (2000) suggests that the reor-ganization of amygdala and prefrontal limbic areas that innervate the hypothalamus and mod-ulate emotional reactivity, as well as alterations in the balance between mesocortical andmesolimbic dopamine systems involved in stress regulation, may drive the reorganization of

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cap heightbase of textthe adolescent brain. Indeed, an increase in the volume of the right hypothalamus (Sowell &

Jernigan, 1998) is seen in late adolescence.An fMRI study indicates that adolescents exhibit greater activation in the amygdala than

in the frontal lobe during the identification of an emotional state from a facial expression, incontrast to adults, who show greater frontal over amygdala activation (Yurgelun-Todd, 1998).These data suggest that the right brain hierarchical dual corticolimbic–autonomic circuits thatsupport self-regulation and stress coping mechanisms are significantly reorganized in adoles-cence (see Figure 3). This allows for early imprinted internal working models of attachmentthat encode strategies of affect regulation to become more complex over the course of theEriksonian stages of the life cycle.

The stress literature clearly suggests that exposing the personality to learning from novelstressors and challenges is “pivotal for emotional and intellectual growth and development”(Chrousos, 1998, p. 312). Yet in addition to being potentially growth enhancing these sameevents can be emotionally overwhelming and disorganizing. However, during disequilibratingstage transitions when right lateralized autoregulatory systems are reorganizing, the child–adolescent with a secure attachment can access emotionally available parents for interactiveregulation. In this manner, the original attachment objects can continue to scaffold the indi-vidual’s developing nascent regulatory capacities.

This same principle is articulated in the neuropsychological literature by Lane, Kivley, DuBois, Shamasundara, and Schwartz:

[I]ndividuals who are naturally right hemispheric dominant may be better able to perceiveand integrate emotion cues from the environment and thus take full advantage of an emo-tionally nurturing environment in promoting emotional development. (1995, p. 535)

Each of these ontogenetic continuations allows for more complex right and right– left repre-sentations, yet the earliest-forming strategies of affect regulation, cocreated in attachment trans-actions of affective synchrony, provide the coping mechanisms for dealing with the stressorsinherent in these later novel, more challenging socioemotional environments. In securely at-tached individuals, or those in interaction with securely attached individuals who can act asinteractive regulators, unconscious internal working models can become more complex.

The experience-dependent expansion of the right brain is reflected in the growth of theunconscious over the lifespan (Schore, 1999d). This reorganization is accompanied by morecomplex interconnections with the also expanding left brain, especially the anterior sections ofthe corpus callosum, which include axons of the orbitofrontal areas that “participate in inter-hemispheric integration on a broad scale” (Cavada et al., 2000). The orbitofrontal and amyg-dalar areas are the most plastic areas of the cortex (Barbas, 1995), and thus capable of futuredendritic and synaptogenetic growth. This major stress coping system in the brain, activatedin contexts of uncertainty, can potentially accrue more complexity.

During the transitions between later developmental stages the individual is presented withthe challenge of retaining continuity while changing in response to environmental pressures.These challenges are associated with positive and negative affective states, and they call for aresilient right orbitofrontal regulated capacity that can read the facially expressed states ofothers, access a theory of mind, as well as cope with, regulate, and thereby tolerate the uncer-tainty and stress that are inherent in the attachment separation and exploratory dynamics ofthese transitional periods. Such regulated interpersonal and intrapersonal experiences allow forthe further experience-dependent maturation of the emotion processing right brain at later stagesof development. The evolutionary progression of the right lateralized frontolimbic “social ed-



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cap heightbase of textitor” (Brothers, 1997) can now reedit more complex yet coherent and adaptive internal working

models that can flexibly process greater amounts of information in more complex subjectivestates. The continuing ontogeny of this self-regulating and self-correcting dynamic systemallows for an expansion of the boundaries of the emotion communicating self. The early rightbrain capacities of processing socioemotional information and bodily states are not only centralto the origin of the self, they are required for the ongoing development of the self over thelifespan.

This evolution of the developmental trajectory allows for an elaboration and increasedcomplexity of the known functions of the right brain: the storage of internal working modelsof the attachment relationship (Schore, 1994), the processing of socioemotional informationthat is meaningful to the individual (Schore, 1998a), the ability to empathize with the emotionalstates of other humans beings (Schore, 1996), the mediation of emotional-imagistic processesin moral development (Vitz, 1990), the appreciation of humor, a mechanism for coping withdaily stress (Shammi & Stuss, 1999), the cerebral representation of one’s own past and theactivation of autobiographical memory (Fink et al., 1996), the establishment of a “personallyrelevant universe” (Van Lancker, 1991), and “the capacity to mentally represent and becomeaware of subjective experiences in the past, present, and future” (Wheeler, Stuss, & Tulving,1997, p. 331).

On the most fundamental level, however, the emotion processing right hemisphere isdominant for the control of vital functions that support survival and enable the organism tocope with stressors (Wittling & Schweiger, 1993). There is now agreement that, fundamentally,“emotion is a mechanism that enables an organism to adapt psychologically, physiologicallyand behaviorally to meet organismic challenges” (Lane, Chua, & Dolan, 1999, p. 996). Thesestressors include interoceptive challenges, because it has been demonstrated that individualsexpress emotional responses to immunological stimuli like bacteria (Kusnecov, Liang, & Shu-rin, 1999). Recall, the emotion-processing right hemisphere is primarily involved with theanalysis of direct information received from the body (Luria, 1973). But in addition, the abilityof the right brain to process exteroceptive socio-emotional stimuli may underlie themechanismby which an individual can recognize and respond to social support that beneficiently altersphysiological processes (Uchino, Cacioppo, & Kielcolt-Glaser, 1996). In an earlier work I haveproposed that the attachment relationship directly influences the development of right brainpsychosocial–neuroendocrine– immune communications (Schore, 1994).

In very recent writings on the relationship between emotional states and physical healthSalovey and his colleagues (2000) conclude,

In general, negative emotional states are thought to be associated with unhealthy patterns ofphysiological functioning, whereas positive emotional states are thought to be associatedwith healthier patterns of responding in both cardiovascular activity and the immune system.(p. 111)

Salovey also contends that to mount an adaptive coping response to preserve mental (andphysical) health, the individual must be able to access “emotional intelligence,” defined as theprocessing of emotional information and accurate perception and appraisal of emotions inoneself and others, appropriate expression of emotion, and adaptive regulation of emotion insuch a manner as to enhance living (Salovey & Mayer, 1989/1990).

This psychological description is echoed in current neuroscience, where Lane et al. con-clude, “as right hemispheric dominance in the perception of facial emotion increases, the abilityto perceive complexity during the processing of emotional information increases” (1995, p.525). In a direct counterpart ot psychological “emotional intelligence,” Brothers (1990) offers

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cap heightbase of textthe neurobiological concept of “social intelligence,” a product of the “social brain” that is

composed of limbic areas of the orbitofrontal cortex and amygdala, and face processing systemsin the temporal lobe. This model is also advanced by Baron-Cohen et al. (2000, p. 355), whodifferentiates general intelligence from social intelliegence, the latter decribed as:

. . . our ability to interpret others’ behaviour in terms of mental states (thoughts, intentions,desires and beliefs), to interact both in complex social groups and in close relationships, toempathize with others’ states of mind, and to predict how others will feel, think, and act.

Recall that limbic circuits are emphasized in specifically the right brain, that the rightlimbic system is more directly connected with subcortical neuochemical systems associatedwith emotion, and that the limbic system is intimately tied to attachment functions. The dataoffered in this work suggest that emotional or social intelligence relies heavily upon right brainfunction, and that this capacity is an outcome of a secure attachment and a central componentof adaptive infant, child, adolescent, and adult mental health.

In a related conception, Gardner (1983) speaks of “personal” intelligence, which has twoforms, intrapersonal intelligence, the ability to access one’s feeling life, and interpersonal in-telligence, the ability to read the moods, intentions, and desires of others. These dual modesrefer to, respectively, right brain autoregulatory and interactive regulatory capacities. As de-scribed above, these two abilities are available to the securely attached individual, and for thisreason such early-appearing coping capacities of adaptive infant mental health are positivefactors for “optimal development” and the ability to increase the complexity of the brain/mind/body self system and thereby enhance and vitalize the experience of being alive over all of thestages of the lifespan.

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